Direct endovascular treatment may be more appropriate for patients with good collateral circulation: a retrospective case-control study

Introduction

Intravenous thrombolysis combined with endovascular treatment (IVT + EVT) is the primary treatment option for patients with acute ischemic stroke due to large-vessel occlusion (AIS-LVO) in the anterior cerebral circulation when symptom onset occurs within 4.5 hours (1). While intravenous thrombolysis (IVT) before endovascular treatment (EVT) may offer benefits, it also carries potential risks (2). Administering IVT may disrupt the blood-brain barrier and affect coagulation, increasing the risk of cerebral hemorrhage (3). Additionally, IVT may lead to thrombus fragmentation, which can impair distal vessel perfusion (4). IVT can also delay the start of EVT and increase healthcare costs (5). This has raised the question of whether it may be preferable to skip IVT and proceed directly to EVT. Recently, studies such as DIRECT-MT (6) and DEVT (2) demonstrated the noninferiority of performing EVT alone compared to IVT + EVT. However, other studies such as SKIP (7), MR CLEAN NO-IV (8), and SWIFT DIRECT (9) did not confirm noninferiority for EVT alone. These varying outcomes reflect the ongoing debate regarding the omission of IVT in favor of direct EVT for treating AIS-LVO. The inconsistent findings suggest that IVT may still provide a benefit for specific patient subgroups, underscoring the need to identify factors that may influence the effectiveness of IVT before EVT. This research lay the groundwork for personalized treatment strategies, allowing the choice between IVT and direct EVT to be tailored to each patient’s unique clinical profile and circumstances.

Previous study has shown that collateral circulation can improve the delivery of thrombolytic agents to the thrombus, and a stronger collateral circulation being associated with higher rates of successful recanalization (10). However, it is still unclear whether collateral status can serve as a reliable criterion for guiding clinical decisions on whether to proceed with EVT alone or IVT + EVT. The primary objective of this study was to assess the impact of collateral status on clinical outcomes in patients receiving EVT alone vs. those receiving IVT + EVT. We present this article in accordance with the STROBE reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-24-322/rc).

Methods

Cohort

We conducted a retrospective analysis of 238 consecutive patients diagnosed with AIS-LVO who underwent EVT, with or without intravenous alteplase at The First Affiliated Hospital of Soochow university, from January 2019 to January 2023. The inclusion criteria of EVT were: (I) age of 18 years or older; (II) acute ischemic stroke due to large-vessel occlusion (LVO), confirmed by computed tomographic angiography (CTA), magnetic resonance angiography (MRA), or digital subtraction angiography (DSA); (III) National Institutes of Health Stroke Scale (NIHSS) score of 6 points or higher. Exclusion criteria included: (I) hemorrhage on the computed tomography (CT) scan; (II) Alberta Stroke Program Early Computed Tomography Score (ASPECTS) below 6; (III) a premorbid modified ranking scale (mRS) score greater than 1; (IV) lack of essential imaging or clinical parameters. Study-specific inclusion criteria were: (I) occlusion of intracranial internal carotid artery (ICA) or segment 1 of the middle cerebral artery (MCA); (II) onset-to-door time within 24 hours, with patients arriving beyond 6 hours meeting DEFUSE 3 criteria (11); and (III) undergoing multi-mode CT. Exclusion criteria were: (I) non-use of Solitaire FR with intracranial support catheter for mechanical thrombectomy (SWIM) as first-line treatment; (II) angiography showing recanalization [modified tissue thrombolysis in cerebral infarction (mTICI) 2b–3]; and (III) treatment with intra-arterial thrombolysis alone.

The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013) and was approved by the Research Ethics Committee of The First Affiliated Hospital of Soochow University (No. 2022/274). The informed consent was obtained from all the patients or their representatives.

Variables

In this study, a comprehensive set of variables was evaluated, including: patient age; gender; mTICI score; presence of hypertension, diabetes, hyperlipidemia; history of smoking; atrial fibrillation; occurrence of a “wake-up” stroke; NIHSS score on admission (12); ASPECTS score (13); tandem occlusion; regional leptomeningeal collateral (rLMC) grade; stroke etiology as per the TOAST criteria (Trial of ORG 10172 in Acute Stroke Treatment), including subtypes such as large artery atherosclerosis (LAA), cardioembolism (CE), and strokes due to other determined or undetermined causes; location of the occlusion (ICA or MCA); onset-to-puncture time (OTP, minutes), which is the time from the stroke onset to the medical procedure; procedure time (PT, minutes); anesthesia mode during the procedure; whether emergency stenting was part of the treatment protocol.

The ASPECTS score was determined from non-enhanced CT images, while the rLMC grade was assessed using CTA. The exact location of occlusion and the presence of tandem occlusion—a combination of intracranial LVO and severe stenosis or occlusion of the ipsilateral extracranial ICA (14), were confirmed via DSA following the EVT procedure (Tables S1-S7).

Collateral status assessment

All patients underwent a non-contrast CT scan of the head using a GE 256-slice CT scanner upon admission. After excluding cerebral hemorrhage, a non-ionic contrast medium (Topromide, Bayer, Germany) was administered via an elbow vein at a rate of 3–5 mL/s. The imaging covered the area from the aortic arch to the vertex, capturing continuous axial slices parallel to the orbitomeatal line. The scan parameters for this procedure were as follows: tube voltage of 120 kV, current of 250 mA, and slice thickness of 0.625 mm.

We employed the collateral grading system as described by Menon et al. (15) using triphasic CTA. The assessment is based on the following criteria: a score of 0 indicates that the artery is not visible, a score of 1 denotes that it is less prominent, and a score of 2 suggests that it is equal to or more prominent compared to a corresponding region in the opposite hemisphere. This evaluation is conducted across six ASPECTS regions (M1–6), which include the anterior cerebral artery region and basal ganglia. Additionally, pial arteries in the Sylvian sulcus are assigned scores of 0, 2, or 4.

Following the methodology established in a previous study (16), the rLMC score is categorized into three groups: “good”, collateral circulation scores of 17 to 20 points; “moderate”, collateral circulation scores 11 to 16; and “poor”, collateral circulation scores of 0 to 10. Two neurologists with over 15 years of experience independently reviewed and assigned scores by consensus, ensuring that they were blinded to any clinical information and follow-up scans.

Outcome measures

The primary outcome of the study was the assessment of patients’ scores on the modified Rankin Scale (mRS) at 90 days, with outcomes classified as either “favorable” (mRS 0–2) or “poor” (mRS 3–6) (17). The secondary outcomes included: mortality within 90 days: referring to the occurrence of death during the 90-day post-treatment period; embolus escape: defined as angiographic distal branch occlusion within the same or a new vascular territory, as specified in reference (18); successful recanalization (19): defined as an mTICI score of 2b–3, indicating effective reperfusion as observed on the final angiography; intracranial hemorrhage (ICH): characterized by the persistent hyperdensity observed on a follow-up CT scan, typically 24 hours or more after the procedure, in accordance with the definition provided in reference (20); symptomatic ICH (sICH): defined as any new ICH detected on follow-up CT images, accompanied by the increase in the NIHSS score of 4 or more within 24 hours, as described in reference (21).

Statistical analysis

The baseline data were stratified based on the treatment approach (EVT alone or IVT + EVT). Descriptive statistics were reported using frequencies and proportions for categorical variables, while continuous variables were expressed as medians and interquartile ranges (IQRs) or means and standard deviations (SDs). Differences between proportions were assessed using the Chi-squared (χ²) test, and comparisons of medians were performed using the Mann-Whitney U test.

The association between the treatment approach (EVT alone or IVT + EVT) and the score on the mRS at 90 days modified by baseline collateral status, were assessed. To evaluate this, multivariable logistic regression was employed to estimate the adjusted common odds ratio for a shift toward better functional outcome on the mRS for EVT alone compared to IVT + EVT.

The analysis was initially conducted on the entire study population. Subsequently, a stratified analysis was performed to account for potential interactions between collateral status (classified as good, moderate, or poor) and treatment approach. Both unadjusted and adjusted models were included, accounting for variables such as age, gender, NIHSS score, ASPECTS score, and OTP. For the secondary outcomes, the same adjustments and analytical strategies were applied as for the primary outcome and unadjusted results were also reported. Odds ratios (ORs) and 95% confidence intervals (CIs) were calculated for all continuous variables based on a 1-unit increase, and for presence of a factor for categorical variables. All the analyses were performed using R software (version 3.6.1), with two-sided P value of less than 0.05 considered statistically significant.

Results

Between January 2019 and January 2023, a total of 341 patients were treated. Of these, 238 patients were included in this study for evaluation, with 80 (33.6%) in the EVT group and 158 (66.4%) in the IVT + EVT group (Figure 1).

Figure 1 Flowchart for patient selection. EVT, endovascular treatment; IVT, intravenous thrombolysis; mRS, modified Rankin Scale; ASPECTS, Alberta Stroke Program Early Computed Tomography Score; M2, segment 2 of middle cerebral artery; NIHSS, National Institute of Health Stroke Scale; SWIM, Solitaire FR with intracranial support catheter for mechanical thrombectomy.

The baseline characteristics of patients are summarized in Table 1. Patients in the IVT + EVT group exhibited a shorter time interval from symptom onset to groin puncture (325.50 vs. 388.50 minutes, P=0.016). However, no significant differences were observed in other baseline characteristics between the two groups. Given the differences in OTP between the groups, we conducted univariate and multivariate analyses separately for the overall patients, the EVT group, and the IVT + EVT group in the subsequent statistical analysis to minimize bias associated with the varying baseline OTP data.

In univariate analysis, patients with good collateral circulation achieved better mRS scores at 90 days and had a higher rate of successful recanalization. They also experienced a lower incidence of ICH, mortality, embolus escape, as well as a higher rate of achieving mTICI 3 recanalization. Notably, there was no statistically significant difference in the occurrence of sICH between these groups (Table 2).

Primary outcome

A multivariate logistic analysis with the inclusion of age, gender, NIHSS score, ASPECTS, OTP, and rLMC demonstrated that patients with good collateral circulation achieved better mRS scores at 90 days (OR, 3.815; 95% CI: 2.112–7.265). Additionally, patients in both the EVT alone group (OR, 8.381; 95% CI: 2.120–46.695) and the IVT + EVT group (OR, 3.157; 95% CI: 1.618–6.541), with better collateral circulation were associated with improved clinical outcomes (Table 3, Table S1).

Secondary outcome

When incorporating age, gender, NIHSS score, ASPECTS, OTP, and rLMC into a multivariate logistic analysis, it was found that patients with good collateral circulation exhibited several significant trends in secondary outcomes: a higher rate of successful recanalization (OR, 3.991; 95% CI: 1.322–16.245); a lower rate of mortality (OR, 0.330; 95% CI: 0.157–0.657); a lower rate of embolus escape (OR, 0.428; 95% CI: 0.188–0.920); a lower rate of achieving mTICI 3 recanalization (OR, 0.532; 95% CI: 0.317–0.876). However, no significant associations were found between good collateral circulation and the occurrence of ICH (P=0.181) or sICH (P=0.794).

The effects of collateral circulation on secondary outcomes differed between the EVT group and the IVT + EVT group: in the EVT group, collateral circulation had no significant impact on ICH (P=0.377), sICH (P=0.543), mortality (P=0.178), embolus escape (P=0.464), successful recanalization (P=0.197), or achieving mTICI 3 recanalization (P=0.370). Conversely, in the IVT + EVT group, better collateral circulation was associated with a higher rate of mortality (OR, 0.334; 95% CI: 0.145–0.725), a higher rate of embolus escape (OR, 0.359; 95% CI: 0.130–0.894), and a lower rate of achieving mTICI 3 recanalization (OR, 0.460; 95% CI: 0.244–0.844). These findings underscore the complex interplay between collateral circulation and treatment outcomes, revealing how this relationship varies between the two treatment groups (Table 3, Tables S2-S7, and Figure 2).

Figure 2 Comparisons in primary and secondary outcomes in the overall patients, EVT group, and EVT + IVT group. Collateral status was classified into three groups: poor, moderate, and good, with poor collateral status set as the reference category. Key variables, including age, gender, OTP, NIHSS score, and ASPECTS, were incorporated into a multivariate analysis to evaluate the impact of collateral status on clinical outcomes. This approach allowed for a more comprehensive assessment of how collateral status, adjusted for relevant covariates, influenced patient prognosis following treatment. mRS, modified Rankin Scale; ICH, intracranial hemorrhage; sICH, symptomatic intracranial hemorrhage; mTICI, modified tissue thrombolysis in cerebral infarction; EVT, endovascular treatment; IVT, intravenous thrombolysis; OR, odds ratio; CI, confidence interval; OTP, onset-to-puncture time; NIHSS, National Institute of Health Stroke Scale; ASPECTS, Alberta Stroke Program Early Computed Tomography Score.

Discussion

The primary finding of this study was that, better collateral circulation was linked to favorable 90-day outcomes in both the EVT group (OR: 8.381, P=0.006) and the IVT + EVT group (OR: 3.157, P=0.001). However, in the IVT + EVT group, better collateral circulation was also associated with an increased mortality rate (OR: 0.334, P=0.007), higher rate of embolus escape (OR: 0.359, P=0.033) and a reduced rate of achieving mTICI 3 recanalization (OR: 0.460, P=0.014). These results suggest that AIS-LVO patients with stronger collateral circulation may derive greater benefit from EVT alone rather than from the combination of IVT and EVT.

The current guidelines for acute ischemic stroke management recommend a combined approach of IVT and EVT as the preferred first-line approach for patients with LVO who present within 4.5 hours of symptom onset (1). This dual approach has demonstrated improved outcomes in this patient population. However, there is ongoing debate on whether it is necessary to forgo IVT prior to EVT or if EVT alone is sufficient. Several studies have sought to clarify this issue. The DIRECT-MT (6) and DEVT (2) trials demonstrated that EVT alone was noninferior to IVT + EVT in terms of achieving favorable functional outcomes (mRS 0–2) at 90 days, suggesting that EVT alone could be a reasonable alternative in certain patients. The DEVT trial, in particular, was stopped early after meeting predefined success criteria, reinforcing EVT alone as a viable option. However, other studies, including SKIP (7), MR CLEAN NO-IV (8), and SWIFT DIRECT (9), did not establish noninferiority or superiority of EVT alone, leaving open the possibility that IVT may benefit certain patient subgroups. A recent analysis by Zhou et al. (22) within the DIRECT-MT trial, attempted to examine whether the site of vessel occlusion could inform the decision to use IVT before EVT. This analysis did not support using occlusion site as a criterion for IVT use in patients eligible for EVT.

Collateral circulation plays a crucial role in sustaining blood flow to ischemic brain regions during an acute stroke particularly by enabling retrograde flow, which can help thrombolytic agents access the occlusion site more effectively. Enhanced collateral flow increases the local concentration of thrombolytic drugs, contributing to improved revascularization chances (23). Prior research has established that patients with good collateral circulation often experience a slower rate of infarct progression, more favorable clinical outcomes, and a reduced risk of hemorrhagic transformation post-IVT (10). This suggests that a potentiating effect of good collateral circulation on IVT’s efficacy. In our study, however, we found that patients with better collateral circulation did not derive additional benefit from the combined IVT + EVT approach over EVT alone. The hypothesis that collateral circulation might amplify the effects of IVT preceding EVT was not supported. Our univariate analysis did show significant differences in OTP between EVT and IVT + EVT groups. To address OTP as a potential confounder, we included it in the multivariate regression analysis across all patient groups. Consistent with Manning et al.’s findings, we observed no significant OTP influence on outcomes after adjustment (24). Interestingly, for patients with better collateral circulation, EVT alone was associated with improved outcomes compared to IVT + EVT. Specifically, in the IVT + EVT group, good collateral circulation correlated with higher mortality (OR: 0.334; 95% CI: 0.145–0.725; P=0.007), an increased rate of embolus escape (OR: 0.359; 95% CI: 0.130–0.894; P=0.033), and a lower frequency of achieving a mTICI score of 3 (OR: 0.460; 95% CI: 0.244–0.844; P=0.014). In contrast, collateral circulation status in the EVT group alone was not significantly associated with mortality, embolus escape, or mTICI 3 outcomes. Notable, despite these differences in secondary outcomes, the primary outcome of improved 90-day prognosis remained consistent across both groups, underscoring the potential for EVT alone as a robust treatment option for patients with strong collateral networks.

The study by Ren et al. (4) [2018] highlighted an increased incidence of clot migration in patients who received bridging IVT prior to EVT, with a migration rate of 18.7%, compared to 3.8% in those who underwent direct EVT. Mohammaden et al. (25) further investigated this association, noting that intravenous tissue-type plasminogen activator (IV-tPA) use during EVT was linked to higher rates of distal clot migration and suggesting that collateral circulation plays a crucial role in this dynamic. This underscores how IVT and collateral status together influence clot behavior and migration in acute ischemic stroke. Our findings suggest good collaterals may enhance the effectiveness of IVT by delivering thrombolytic drugs to the occluded site more effectively, which could improve the rate of successful vascular recanalization. However, this may also promote microemboli escape during subsequent EVT, leading to an increased incidence of embolus escape in patients with good collateral circulation within the IVT + EVT group. This elevated rate of embolus escape may contribute to the lower incidence of complete revascularization (mTICI 3) in patients with good collateral circulation within the IVT + EVT group, potentially explaining the observed increase in mortality (26). Our results, aligned with another study showing that patients who achieve mTICI 2b reperfusion experience higher mortality rates than those achieving mTICI 3, emphasizing the impact of collateral circulation and clot migration on treatment outcomes in patients receiving IVT + EVT. This complex interplay suggests that patients with robust collaterals may, paradoxically, benefit more from EVT alone, avoiding the potential for increased microemboli escape associated with prior IVT.

The observation that good collateral circulation was linked to poorer secondary outcomes in the IVT + EVT group, despite better primary outcomes in both treatment groups, indeed suggests that collateral circulation could play a strategic role in selecting the most suitable treatment approach. This finding supports the notion that collateral status could guide clinicians in deciding whether to pursue EVT alone or the combined IVT + EVT strategy. For patients with good collateral circulation who are candidates for IVT + EVT, implementing specific measures to mitigate embolus escape may be beneficial. Utilizing advanced techniques, such as a balloon guiding catheter, which can reduce distal embolization by temporarily occluding blood flow during clot retrieval, could be advantageous. Additionally, employing newer-generation mechanical thrombectomy devices with improved clot engagement and capture could further enhance procedural outcomes and reduce the risk of embolic complications.

There are some limitations that warrant consideration in this study. First, as a single-center retrospective study conducted over an extended period, selection bias may have influenced the findings. Future large-scale, multi-center prospective studies would be valuable to strengthen clinical evidence and mitigate this limitation. Second, thrombus characteristics, which can influence the response to IVT and subsequently affect EVT outcomes, were not analyzed. The retrospective nature of this study precluded the collection of thrombus specimens necessary for this analysis (27). Third, variability in collateral circulation assessment may arise due to differences in the timing of image acquisition relative to contrast media injection (28). Fourthly, the study excluded patients with A1 occlusions, as only three cases were treated with EVT at our center during the study period. Lastly, all patients received thrombectomy using the combined Solitaire FR with intracranial support catheter for mechanical thrombectomy (SWIM) technique. Data on alternative thrombectomy methods, such as direct aspiration or other stent retrievers, were not collected, limiting the generalizability of the results across different thrombectomy techniques. Further research is necessary to assess whether these findings extend to other methods.

Conclusions

In conclusion, better collateral circulation is associated with favorable 90-day outcomes in both EVT and IVT + EVT groups. However, in the IVT + EVT group, better collateral circulation was linked to higher mortality, increased embolus escape, and lower rates of achieving mTICI 3 recanalization. These findings suggest that patients with AIS-LVO and robust collateral circulation may derive greater benefit from EVT alone. Our study provides a theoretical foundation for future multicenter trials, proposing that collateral circulation status could serve as a potential indicator for determining the need for IVT prior to mechanical thrombectomy.

Acknowledgments

We thank professor Feng Zhang, MD, PhD, Department of Radiology, University of Washington School of Medicine, Seattle, Washington, USA, for helping to edit the manuscript and enhance the clarity, understandability, and readability.

Funding: This study was supported by grant from Jiangsu Medical Association of China [No. SYH-3201140-0087(2023034)].

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-24-322/rc

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-24-322/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are 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. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013) and was approved by the Research Ethics Committee of The First Affiliated Hospital of Soochow University (No. 2022/274). Informed consent was obtained from all the patients or their representatives.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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