Abstract
Background
The value of clot imaging in patients with emergent large vessel occlusion (ELVO) treated with thrombectomy is unknown.
Methods
We performed retrospective analysis of clot imaging (clot density, perviousness, length, diameter, distance to the internal carotid artery (ICA) terminus and angle of interaction (AOI) between clot and the aspiration catheter) of consecutive cases of middle cerebral artery (MCA) occlusion and its association with first pass effect (FPE, TICI 2c-3 after a first attempt).
Results
Patients (n = 90 total) with FPE had shorter clot length (9.9 ± 4.5 mm vs. 11.7 ± 4.6 mm, P = 0.07), shorter distance from ICA terminus (11.0 ± 7.1 mm vs. 14.7 ± 9.8 mm, P = 0.048), higher perviousness (39.39 ± 29.5 vs 25.43 ± 17.6, P = 0.006) and larger AOI (153.6 ± 17.6 vs 140.3 ± 23.5, P = 0.004) compared to no-FPE patients. In multivariate analysis, distance from ICA terminus to clot ≤13.5 mm (odds ratio (OR) 11.05, 95% confidence interval (CI) 2.65–46.15, P = 0.001), clot length ≤9.9 mm (OR 7.34; 95% CI 1.8–29.96, P = 0.005), perviousness ≥ 19.9 (OR 2.54, 95% CI 0.84–7.6, P = 0.09) and AOI ≥ 137°^ (OR 6.8, 95% CI 1.55–29.8, P = 0.011) were independent predictors of FPE. The optimal cut off derived using Youden’s index was 6.5. The area under the curve of a score predictive of FPE success was 0.816 (0.728–0.904, P < 0.001). In a validation cohort (n = 30), sensitivity, specificity, positive and negative predictive value of a score of 6–10 were 72.7%, 73.6%, 61.5% and 82.3%.
Conclusions
Clot imaging predicts the likelihood of achieving FPE in patients with MCA ELVO treated with the aspiration-first approach.
Keywords: Thrombectomy, first pass effect, perviousness, endovascular, stroke
Introduction
Direct aspiration, often referred to as ADAPT (A Direct Aspiration First Pass Technique), is a simple and cost-effective approach for the treatment of emergent large vessel occlusion (ELVO) in acute ischemic stroke (AIS). 1 Primary aspiration without the need of rescue stent retriever devices is achieved in 65–71% of cases.2–4 Predicting which patients would benefit from aspiration alone technique can be highly valuable in selection of the most appropriate approach for mechanical thrombectomy. However, this has proven to be a challenging task. According to several independent studies, National Institutes of Health Stroke Scale (NIHSS) score, use of intravenous alteplase, location of ELVO, hyperdense vessel sign, or clot length are not predictive of recanalization outcome with aspiration alone.5–7 Yet, others have shown that site of occlusion, vessel angulation and clot burden may be associated with the effective aspiration.7–9
Despite such extensive prior research on this topic, most of the proposed factors that seem to affect recanalization success have been studied individually. Furthermore, how these findings could be applied to individual cases of endovascular thrombectomy with aspiration-first approach remains unknown. In this study, we performed retrospective analysis of a wide range of baseline imaging characteristics (clot density, perviousness, length, diameter, distance to the internal carotid artery [ICA] terminus and angle of interaction [AOI] with the aspiration catheter) of consecutive cases of AIS from anterior circulation ELVO to determine its association with success or failure of aspiration-first component. We also propose a predictive scale based on clot imaging markers that is predictive of first pass effect (FPE) achieved with aspiration thrombectomy.
Methods
Patient population
This study was approved by the local institutional review board of the two participating centers for retrospective data collection and review with waivers for informed consent. Consecutive cases of AIS with angiographic evidence of the middle cerebral artery M1 and M2 occlusion diagnosed on computed tomography angiography (CTA) who were treated with the direct aspiration approach between July 2018 and December 2019 were included in this study. Cases with significant artifact or poor contrast opacification on CTA precluding accurate analysis, cases with regions of Hounsfield unit (HU) values >100 representing calcifications, or with baseline MRA were excluded from analysis. Both centers utilized a similar treatment approach as described previously. 1 Briefly, after placing a long sheath into the distal cervical internal carotid artery, a large bore 0.070–0.072″ aspiration catheter (6 F Sofia [MicroVention], Jet 7 [Penumbra], React-71 [Stryker]), was advanced over 0.025–0.035″ microcatheter and 0.014–0.016″ microwire close to the proximal aspect of the clot. Aspiration was performed by connecting to continuous aspiration pump. In cases when aspiration alone was not successful, stent retriever thrombectomy was performed next in conjunction with continuous aspiration via the large-bore aspiration catheter.
Imaging analysis
Imaging analysis was performed locally by each participating center. Thrombus HU density, perviousness, length, angle of interaction and distance from ICA terminus were quantified as previously described (Figure 1).9–11 Briefly, to calculate density and perviousness, and clot length, noncontrast computed tomography (NCCT) and CTA were co-registered and three separate regions of interest were placed in the proximal, middle and distal part of the thrombus to calculate the mean HU density value of the affected side. CTA images were manually aligned with NCCT images to ensure that the corresponding measurements were collected from the same imaging plane. Clot length was assessed by co-registering NCCT with CTA. In cases of clot extending into multiple middle cerebral artery (MCA) bifurcation or trifurcation branches, the longest M2 clot was used for calculations. Distance from ICA terminus was calculated using axial, coronal or sagittal views to measure cumulative distance from ICA terminus to the beginning of the clot. AOI was measured between the major axes of the aspiration catheter and the clot using CTA and intraprocedural digital subtraction angiogram (DSA) images. Imaging analysis was conducted by operators blinded to the knowledge of final angiographic or clinical outcome except for knowledge of stroke laterality. Inter-rater variability assessment of imaging characteristics was assessed using kappa test.
Figure 1.
Examples of clot imaging measurements: (a) noncontrast computed tomography (NCCT) and (b) computed tomography angiography (CTA) axial images are co-registered to place three separate regions of interest (ROI) at the proximal, middle and distal parts of the clot in order to measure its density in Hounsfield units (HU) and calculate perviousness (later is defined as difference in HU values between CTA and NCCT); (c) CTA, coronal view, showing measurements of clot length and ICA distance to clot. Clot length (double arrow, a) was measured using the largest extension of the filling defect on CTA. To accurately estimate distance from ICA terminus to proximal end of the clot (double arrow, b), when applicable, a cumulative measured axial, coronal and sagittal CTA views was performed (not shown here, given adequate representation of distance on axial CTA image alone); (d) digital subtraction angiogram (DSA), baseline image of road map and postaspiration thrombectomy. The position of the aspiration catheter at the occlusion site is shown. Angle of interaction is the angle between the aspiration catheter and the clot (dotted lines) using measurements obtained from pre-thrombectomy, working projections and final post-thrombectomy images.
Outcome measures
Angiographic assessments of thrombectomy procedures were evaluated using the thrombolysis in cerebral infarction (TICI) grading scale with the addition of the 2c score (2b defined as 50–89% reperfusion; TICI 2c as 90–99% reperfusion and TICI 3 as 100% reperfusion of the affected territory, respectively). 12 FPE was defined as TICI 2c/3 recanalization after a first aspiration thrombectomy attempt. 13
Statistical analysis
Descriptive analysis was performed. Distribution of data was assessed using Shapiro-Wilk test. Continuous data with normal distribution was presented as means and standard deviation, and median and interquartile ranges for data with non-normal distribution were reported. Categorical variables were presented as percentage and proportions. Patients were divided into two groups based on the achievement of FPE. The two groups were compared for baseline characteristics, using independent T test and Chi square tests for continuous and categorical data respectively.
We then carried out a multivariate regression analysis to identify independent predictors of FPE. Variables with a P value of <0.1 were included in the multivariate model. In order to calculate a cut off with best sensitivity and specificity of independent predictors, we performed receiver operator curve analysis. The cutoffs with the best sensitivity and specificity were estimated using Youden index. We calculated relative odds for FPE based on the cut off using multivariate regression analysis. Each variable was then assigned a score based on the relative odds ratio. Number of patients with FPE in each score category was calculated. Optimal score for the prediction of FPE was calculated using Youden’s J index. Sensitivity, specificity, positive and negative predictive values were calculated for the highest score category. The score cut off was tested in validation cohort of consecutive mechanical thrombectomy patients. Statistical analysis was carried out using SPSS v 25 (IBM, Chicago IL). A P value of <0.05 was considered significant.
Results
Ninety patients were included in the study to analyze clot imaging characteristics associated with FPE of aspiration thrombectomy. Of these, 56 (61.5%) patients were female. Mean age of the cohort was 72.5 ± 15.3 years, median NIHSS was 16.5 (IQR 8–22) and mean time from symptom onset to puncture was 229.9 ± 166.5 min. Thirty-nine (42.8%) patients achieved a FPE (mTICI of 2c and 3 after first pass). There was no difference between patients with and without FPE with respect to gender proportion, mean age, comorbidities, use of IV alteplase use, baseline NIHSS score, laterality and location of LVO (Table 1).
Table 1.
Comparison of baseline characteristics of patients with and without first pass effect.
| Variable | First pass effect (N = 39) | No first pass effect (N = 51) | P value |
|---|---|---|---|
| Demographic and clinical data | |||
| Male, n (%) | 12 (30.8) | 22 (43.1) | 0.23 |
| Female, n (%) | 27 (69.2) | 29 (56.9) | |
| Age, mean ± SD | 75.3 ± 15.1 | 70.31 ± 15.2 | 0.13 |
| Hypertension, n (%) | 31 (79.5) | 37 (72.5) | 0.54 |
| Diabetes mellitus, n (%) | 9 (23.1) | 12 (23.5) | 0.92 |
| Dyslipidemia, n (%) | 19 (48.7) | 21 (41.2) | 0.53 |
| Congestive cardiac failure, n (%) | 3 (7.7) | 8 (15.6) | 0.24 |
| Atrial fibrillation, n (%) | 14 (35.9) | 21 (41.2) | 0.59 |
| Current smoke, n (%) | 6 (15.4) | 7 (13.7) | 0.85 |
| Previous stroke, n (%) | 8 (20.5) | 15 (29.4) | 0.31 |
| NIHSS score, mean ± SD | 16.2 ± 7.1 | 15.3 ± 7.9 | 0.61 |
| Treatment details | |||
| IV alteplase, n (%) | 24 (61.5) | 27 (52.9) | 0.28 |
| Time from symptom onset to puncture, minutes, mean ± SD | 228.1 ± 201.5 | 231.7 ± 126.4 | 0.9 |
| Number of patients with symptom to puncture >6 h, n (%) | 25 (65.8) | 17 (43.6) | 0.05 |
| Imaging findings | |||
| Right-sided occlusion, n (%) | 26 (66.7) | 24 (47.1) | 0.06 |
| MCA M1 occlusion, n (%) | 33 (84.6) | 32 (62.7) | 0.06 |
| MCA M2 occlusion, n (%) | 6 (15.4) | 18 (35.3) | |
| Clot length (mm) | 9.9 ± 4.5 | 11.7 ± 4.6 | 0.07 |
| Clot density, HU | 43.1 ± 11.2 | 40.9 ± 11.3 | 0.32 |
| Clot perviousness | 39.38 ± 29.5 | 25.43 ± 17.6 | 0.006 |
| Clot diameter (mm) | 2.65 ± 0.67 | 2.8 ± 0.58 | 0.31 |
| Angle of clot/aspiration catheter (°) | 153.6 ± 17.6 | 140.3 ± 23.5 | 0.004 |
| Distance from ICA terminus (mm) | 11.0 ± 7.1 | 14.7 ± 9.8 | 0.048 |
HU: Hounsfield unit; ICA: internal carotid artery; IV: intravenous; NIHSS: National Institutes of Health Stroke Scale; MCA: middle cerebral artery; SD: standard deviation.
In comparison with no-FPE patients, FPE patients had shorter clot length and shorter distance from internal carotid artery (ICA) terminus (9.9 ± 4.5 mm vs 11.7 ± 4.6 mm, P = 0.07 and 11.0 ± 7.1 mm vs 14.7 ± 9.8 mm, P = 0.048, respectively). Mean perviousness of FPE patients was higher than of no-FPE patients (39.39 ± 29.5 vs 25.43 ± 17.6, P = 0.006), and patients with FPE had a larger mean angle to the clot, i.e., 153.6 ± 17.6 vs 140.3 + 23.5, P = 0.004 in no-FPE patients. The Kappa coefficient for agreement in categorizing clots into high and low perviousness clots was 0.43 which indicates moderate agreement.
Based on the criteria defined in the methods section, five variables were included in the multivariate regression model. Of these, clot length, perviousness, distance from ICA terminus, and catheter angle to the clot were independent predictors of FPE (Table 2). Laterality was not found to be a significant predictor of FPE (Table 2).
Table 2.
Predictors of first pass effect.
| Variable | Odds ratio [95% CI] | P value | Optimal cut off for FPE prediction |
|---|---|---|---|
| Right side | 0.41 [0.15–1.13] | .084 | NA |
| Clot length | 0.86 [0.75–0.98] | .027 | ≤9.9 mm |
| Perviousness | 1.02 [1.001–1.05] | .044 | ≥19.9 |
| Distance from ICA terminus to clot | 0.91 [0.850–0.98] | .009 | ≤13.5 mm |
| Angle of clot/aspiration catheter | 1.03 [1.01–1.06] | .007 | ≥137° |
| Constant | .064 | .180 | NA |
CI: confidence interval; ICA: internal carotid artery; NA: not applicable.
Area under the curve (AUC) for perviousness as predictor of FPE was 0.65 (95% CI, 0.53–0.76; P = 0.018) while AUC for clot length was 0.38 (95% CI, 0.26–0.49; P = 0.05), and for angle to the clot AUC was 0.68 (95% CI, 0.56–0.79; P = 0.004).Cut offs with the best sensitivity and specificity for FPE prediction for clot length was ≤9.9 mm while for angle to the clot, perviousness, and clot distance from ICA terminus were ≥137, ≥19.9 and ≤13.3 mm, respectively. In the proposed score, distance from the ICA terminus ≤13.5 mm was assigned four points; clot length ≤9.9 mm was assigned three points; angle to the clot ≥137 was assigned two points; and perviousness ≥19 was assigned one point (Table 3). The score ranged from 0 to 10. Average score was 5.6 ± 2.6 while median was 6 (IQR 4–7). The score showed strong correlation with FPE (Figure 2). Percentage of patients with FPE for each score category is shown in Table 4. All 13 patients with a score of 8–10 achieved FPE while none of the 11 patients with a score of 0–2 had FPE.
Table 3.
Multivariate analysis and first pass effect predictive score.
| Variable | Odds ratio | 95% CI | P value | Assigned score |
|---|---|---|---|---|
| Distance from the ICA terminus ≤13.5 mm | 11.05 | 2.65–46.15 | 0.001 | 4 |
| Clot length ≤9.9 mm | 7.34 | 1.8–29.96 | 0.005 | 3 |
| Angle to the clot ≥137° | 6.8 | 1.55–29.8 | 0.011 | 2 |
| Perviousness ≥19.9 | 2.54 | 0.84–7.6 | 0.09 | 1 |
CI: confidence interval; ICA: internal carotid artery.
Figure 2.
Angiographic outcomes of first pass effect according to the predictive score.
FPE: first pass effect.
Table 4.
First pass effect predictive scoring.
| Total score (N of patients within each score) | No first pass effect (n/N total, %) | First pass effect (n/N total, %) |
|---|---|---|
| 0 (4 patients) | 4/4 (100%) | 0/4 (0%) |
| 1 (4 patients) | 4/4 (100%) | 0/4 (0%) |
| 2 (3 patients) | 3/3 (100%) | 0/3 (%) |
| 3 (7 patients) | 5/7 (71%) | 2/7 (29%) |
| 4 (8 patients) | 7/8 (88%) | 1/8 (12%) |
| 5 (10 patients) | 5/10 (50%) | 5/10 (50%) |
| 6 (22 patients) | 16/22 (73%) | 6/22 (27%) |
| 7 (19 patients) | 7/19 (37%) | 12/19 (63%) |
| 8 (1 patient) | 0/1 (0%) | 1/1 (100%) |
| 9 (1 patient) | 0/1 (0%) | 1/1 (100%) |
| 10 (11 patients) | 0/11 (0%) | 11/11 (100%) |
Scoring: Distance from the ICA terminus ≤13.5 mm is four points; clot length ≤9.9 mm is three points; angle to the clot ≥137 is two points; perviousness ≥19 is one point.
The AUC for the score as predictive of FPE success was 0.816 (0.728–0.904, P < 0.001). The optimal cut off derived using Youden’s index was 6.5. The association of a score 7–10 with FPE success was then tested in the validation cohort. The sensitivity and specificity of a score of 7–10 for FPE were 78.1% and 74.1%, respectively, with positive and negative predictive values of 64.1% and 85.1%, respectively. A score of 6 and above had 96% sensitivity and 44.4% specificity.
The validation cohort consisted of additional 30 consecutive patients with MCA M1 or M2 occlusion who underwent mechanical thrombectomy with aspiration first approach. Of these, 13 patients (13/30; 43.3%) achieved FPE. A score of 7–10 had a sensitivity and specificity of 66.7% and 62.5%, respectively, while the positive and negative predictive values were 30.8 and 88.2%, respectively. Sensitivity and specificity of a score of 6–10 were 72.7 and 73.6%, respectively, while positive and negative predictive values for 61.5 and 82.3%, respectively.
Discussion
The main finding in our study is that multiple imaging clot characteristics are associated with the likelihood of achieving FPE in patients with anterior circulation ELVO treated with the aspiration-first approach. While several studies have looked at individual imaging features in patients treated with aspiration thrombectomy, to our knowledge, this is the first study that attempted to provide a comprehensive review of multiple imaging features and quantify the degree of association of each imaging feature of aspiration thrombectomy success or failure. Based on our analysis, distance from the ICA terminus to the proximal end of the clot and clot length had the strongest association with FPE, followed by the angle of aspiration catheter to the clot and clot perviousness, whereas as clot density and diameter showed no association with angiographic outcome.
There are several potential explanations regarding how these imaging features affect the efficacy of aspiration thrombectomy alone. In the MR CLEAN registry, neither clot length or perviousness showed an association with final reperfusion, and a non-significant trend of an increased chance of successful reperfusion with a more distal thrombus location was observed. 10 Because stent retrieve thrombectomy was the primary treatment modality in the majority of patients (75%) in the MR CLEAN registry, this may explain the contradictory findings of clot length and distance to ICA terminus effects on angiographic outcomes between our study and the MR CLEAN registry investigators. In addition to an increased potential for clot breakdown and/or loss from its tip when withdrawing the aspiration catheter in cases of longer and more distally located clots, there may be differences in clot composition and stroke etiology. Dutra et al. showed that comparing NCCT and CTA characteristics, cardioembolic strokes and non-cardioembolic strokes vary in clot length and distance from ICA terminus to clot. 14 In vitro analysis indicates that clot composition affects the degree of complete clot ingestion or fragmentation during aspiration thrombectomy. 15 Also, more distal clots may have less accurate visualization of the precise clot location as a result of decreased contrast opacification during angiography, resulting in suboptimal contact of the tip of the aspiration catheter with the clot.
The angle of interaction between the aspiration catheter and clot as a predictor of thromboaspiration efficacy was first show by Bernava et al. in a study of 85 patients treated with aspiration thrombectomy. 9 While the authors evaluated final recanalization result and number of passes rather than FPE, their findings of an angle of interaction ≥125.5° as the most accurate cut-off to predict final success or failure is similar to our results of 137° angle for best sensitivity and specificity. One limitation of this imaging marker is that two-dimensional angle measurements are less accurate than using center lines from three-dimentional reconstructions. Finally, the association of perviousness and aspiration thrombectomy has not been previously studied. Perviousness serves as a potential marker of red blood cell and fibrin clot content, and showed strong association with the degree of recanalization with IV alteplase alone.15,16 However, it failed to predict FPE in patients treated with stent retriever thrombectomy. 17 Our data demonstrate that perviousness rather that clot density measured on NCCT alone is predictive of FPE.
In summary, using our predictive scoring system, we conclude that patients with a score in the 7–10 range have a high chance of achieving FPE with aspiration alone. With a score <7, the likelihood of FPE is greatly reduced. Using our data on the optimal cut-off of 6.5, our future research will focus on studying whether the stent retriever-first approach (with or without concurrent aspiration) is more likely to achieve FPE than direct aspiration alone.
Limitations
Our study has several limitations. First, these findings are only applicable to patients with proximal MCA occlusions. We excluded patients from distal MCA occlusions as many imaging markers could not be reliably measured in this population of patients. Also, cases of posterior circulation ELVO were excluded. Second, imaging analysis was performed locally at each center. Although kappa for inter-operator agreement was moderate, 18 the images were not adjudicated by an independent core laboratory, creating the possibility of miscalculating clot imaging findings between the two centers and angiographic results of thrombectomy experiments. The proposed score was not validated in an independent cohort. The score needs to be externally validated before it can be recommended for wider use, however, the proposed score provides a reflection of relative weightage of various imaging characteristics in predicting FPE.
Measuring imaging clot characteristics included in our analysis is a time-consuming process, thus limiting its clinical utility at the present time. However, with the advancement of convolutional neural networks, it is becoming feasible to measure such characteristics in an automated matter. 19 Our group is currently working on creating automated imaging protocols of clot radiomics analysis.
Next, the balloon guide catheter (BGC) is sometimes used in conjunction with aspiration, with studies indicating its independent association on FPE.20,21 Our consecutive patients did not have a BGC used during interventions.
Histological analysis of retrieved clots can provide additional valuable findings on the potential association of clot composition, its radiographic appearance, etiology of ELVO and radiographic and clinical treatment outcomes.22,23 Histological analysis was not included in our study.
Finally, our study was not designed to compare the effectiveness of aspiration and stent retriever thrombectomy in patients with certain clot imaging characteristics. Ultimately, a question that needs to be answered is which one of the two treatments (aspiration-first or stent-retriever first) is more likely to achieve FPE rather than studying the association of imaging clot characteristics individually in patients undergoing one type of treatment alone. Achieving this task will likely require multiple independent analyses conducted using in vitro 3D models (to accurately replicate thrombectomy using both treatment approaches), as well as clinical data before an accurate and reliable imaging grading scale could be incorporated into clinical-decision making when choosing the best thrombectomy option in each individual patient with AIS from ELVO.
Conclusions
Multiple imaging clot characteristics are associated with the likelihood of achieving FPE in patients with anterior circulation ELVO treated with the aspiration-first approach. A predictive scale based on such imaging markers shows excellent correlation with FPE. Further validation of this scoring system in an independent cohort of patients treated with aspiration thrombectomy is warranted.
Footnotes
Declaration of conflicting interests: The author(s) declared the following potential conflicts of interest with respect to the research, authorship, and/or publication of this article: MM—Grants: Principal investigator NIH R21NS109575 Consultant: Medtronic, Canon Medical, Cerenovus Stock options: Serenity medical, Synchron, Endostream, VICIS AHS—Financial Interest/Investor/Stock Options/Ownership: Amnis Therapeutics, Apama Medical, BlinkTBI, Inc, Buffalo Technology Partners, Inc., Cardinal Health, Cerebrotech Medical Systems, Inc, Claret Medical, Cognition Medical, Endostream Medical, Ltd, Imperative Care, International Medical Distribution Partners, Rebound Therapeutics Corp., Silk Road Medical, StimMed, Synchron, Three Rivers Medi- cal, Inc., Viseon Spine, Inc. Consultant/Advisory Board: Amnis Therapeutics, Boston Scientific, Canon Medical Systems USA, Inc., Cerebrotech Medical Systems, Inc., Cerenovus, Claret Medical, Corindus, Inc., Endostream Medical, Ltd, Guidepoint Global Consulting, Imperative Care, Integra, Medtronic, Micro- Vention, Northwest University—DSMB Chair for HEAT Trial, Penumbra, Rapid Medical, Rebound Therapeutics Corp., Silk Road Medical, StimMed, Stryker, Three Rivers Medical, Inc., VasSol, W.L. Gore & Associates. National PI/Steering Committees: Cerenovus LARGE Trial and ARISE II Trial, Medtronic SWIFT PRIME and SWIFT DIRECT Trials, MicroVention FRED Trial & CONFIDENCE Study, MUSC POSITIVE Trial, Penumbra 3D Separator Trial, COMPASS Trial, INVEST Trial. EIL – Consultant: Penumbra, NextGen Biologics, Rapid Medical, Cognition Medical, Three Rivers Medical, Stryker, MedX, Endostream Medical. VMT—Principal investigator: National Science Foundation Award No. 1746694 and NIH NINDS award R43 NS115314-0. Awardee of the abovementioned Clinical and Translational Science Institute grant and Cummings Foundation grant. Co-founder: Neurovascular Diagnostics, Inc. JMD – Research grant: National Center for Advancing Translational Sciences of the National Institutes of Health under award number KL2TR001413 to the University at Buffalo. Consulting: Medtronic; Honoraria: Neurotrauma Science, LLC; shareholder/ownership interests: Cerebrotech, RIST Neurovascular. KS – Consulting: Canon Medical Systems Corporation, Penumbra Inc., Medtronic, and Jacobs Institute. Co-Founder: Neurovascular Diagnostics, Inc Other authors – None.
Funding: The author(s) disclosed receipt of the following financial support for the research, authorship and/or publication of this article: This work was supported by NIH (Grant no. NIH R21NS109575).
ORCID iDs: Muhammad Waqas https://orcid.org/0000-0003-4500-7954
Elliot Pressman https://orcid.org/0000-0002-5160-802X
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