Prevalence, clinical characteristics, and outcomes of carotid web in Chinese patients with acute ischemic stroke due to intracranial large vessel occlusion

Introduction

Identifying the etiology of stroke is crucial for effective secondary prevention. In Asian populations, large vessel occlusion (LVO) is predominantly attributed to intracranial atherosclerosis; however, embolic mechanisms also significantly contribute to its occurrence (1). Notable sources of emboli include cardioembolic events and ruptured atherosclerotic plaques from both extracranial and intracranial large arteries, commonly termed arteriogenic embolisms (2). Of particular note is the higher incidence of cryptogenic embolic strokes in younger cohorts, underscoring the complexity of their diagnosis and management (3).

The carotid web (CaW) represents an atypical form of fibromuscular dysplasia (FMD), primarily affecting the intima of the arterial wall, distinct from traditional atherosclerotic pathologies affecting the extracranial carotid artery (4). This condition is characterized by a fibrous, shelf-like intimal projection that originates from the posterior wall of the internal carotid artery bulb, extending into the arterial lumen (4). Recent studies have suggested that CaW may be a potential underlying cause of embolic stroke of undetermined source, particularly in cases of LVO (5).

The prevalence of CaW in LVO cases is relatively under-documented, with existing research indicating its association in approximately 0.7% to 13.5% of such cases (5-8). Most of these studies focus predominantly on Caucasian populations, revealing a gap in the demographic scope of current research. The incidence of CaW has shown variability across racial groups, with higher occurrences noted in African Americans (4,9). However, comprehensive data on the prevalence and clinical implications of CaW in Asian populations remain limited, with a reported prevalence of symptomatic CaW of 1.5% (2/132) (10).

This study aims to bridge this knowledge gap by exploring the prevalence, clinical characteristics, and outcomes of thrombectomy for symptomatic CaW-associated anterior intracranial LVO within a Chinese cohort. The findings are intended to enhance understanding and guide the clinical management of this complex vascular condition. We present this article in accordance with the STROBE reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-24-2426/rc).

Methods

Study design and participants

This retrospective study analyzed all consecutive cases of anterior circulation LVO ischemic strokes treated with mechanical thrombectomy at two stroke centers in China from January 2018 to June 2024. The inclusion criteria included patients aged ≥18 years with acute anterior circulation LVO within 6 hours of onset, who had a pre-stroke modified Rankin Scale (mRS) score of 0–1, a National Institutes of Health Stroke Scale (NIHSS) score >6, and an Alberta Stroke Program Early CT Score (ASPECTS) ≥6. Patients presenting within a 6–16-hour window were included if they met the DAWN or DEFUSE 3 criteria (11,12) and those within a 16–24-hour window were included if they met the DAWN criteria (11).

Data collection

Patient demographics, cardiovascular risk factors, baseline NIHSS scores, intravenous thrombolysis status, ASPECTS, timing of endovascular treatment, occlusion site, number of thrombectomy attempts, modified Thrombolysis in Cerebral Infarction (mTICI) scores, and pre-stroke and 3-month follow-up mRS scores were systematically recorded. Data on secondary prevention treatment for each case were also collected. Successful recanalization was characterized as mTICI 2b or 3.

Stroke work-up and diagnostic evaluation

Stroke etiology was classified according to the Trial of ORG 10172 in Acute Stroke Treatment criteria (13). To ensure accurate classification of stroke etiology and rule out other potential causes beyond CaW, a comprehensive stroke work-up was conducted for all patients, particularly those suspected of having CaW. Continuous electrocardiographic (ECG) monitoring was performed for a minimum of 72 hours to detect paroxysmal arrhythmias, with a specific focus on atrial fibrillation. For patients without detected arrhythmias during hospitalization, 24-hour Holter monitoring was conducted post-discharge to identify any cardiac sources of embolism that may have gone undetected.

Comprehensive laboratory testing was undertaken to rule out hypercoagulable states. This included assessments for antiphospholipid antibodies, deficiencies in protein C and protein S, antithrombin III levels, and genetic thrombophilias, such as the factor V Leiden mutation and prothrombin gene mutation. Additionally, homocysteine levels were measured to evaluate the potential contribution of hyperhomocysteinemia. All patients also underwent transthoracic echocardiography (TTE) or transesophageal echocardiography (TEE) to detect possible cardioembolic sources, such as a patent foramen ovale or left atrial thrombus.

CaW was diagnosed using digital subtraction angiography (DSA), which identified a thin, shelf-like luminal projection originating from the posterior wall of the carotid bulb. Doppler carotid ultrasound, computed tomography angiography (CTA), and magnetic resonance angiography (MRA) were used to support the diagnosis, rule out carotid dissection, and detect atherosclerotic plaques. DSA images were independently reviewed by two experienced neuroradiologists, and any discrepancies were resolved through consensus.

Brain magnetic resonance imaging (MRI) was performed on all patients to assess for additional ischemic lesions or vascular abnormalities, with special attention given to differentiating embolic stroke from other stroke subtypes.

The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. This study was deemed exempt by the ethics committee’s board for a formal IRB request, and individual consent for this retrospective analysis was waived.

Statistical analysis

Demographic data and clinical information were presented as medians and interquartile range (IQR) due to their non-normal distributions. Continuous variables were compared between patients with and without symptomatic CaW using the Mann-Whitney U test, while categorical variables were compared using the Pearson χ² test or Fisher’s exact test. A two-tailed P value of <0.05 was considered statistically significant. Binary logistic regression analysis was conducted, adjusting for variables such as age, occlusion site, and recanalization status. All data analyses were performed using SPSS software (version 26.0; IBM Corp, Armonk, NY, USA).

Results

During the study period, a total of 515 patients with LVO underwent mechanical thrombectomy. After excluding 103 cases of posterior circulation stroke and 11 cases with incomplete or missing data, 401 patients with acute anterior circulation LVO were included in the final analysis (Figure 1). Among these, 16 patients had symptomatic CaW [3.99%; 95% confidence interval (CI): 2.09–5.89%], with 15 cases being unilateral and 1 case bilateral. Among the confirmed CaW cases, carotid ultrasound was utilized as an adjunctive diagnostic modality in 12 (75.0%) patients, and CTA was performed in 10 (62.5%) patients. In one case, there was diagnostic uncertainty between an ulcerated plaque and CaW, but postoperative histopathology following carotid endarterectomy (CEA) confirmed the presence of CaW. No cases of CaW mimics—such as secondary iatrogenic arterial dissection following mechanical thrombectomy—were observed.

Figure 1 Patients selection flow chart. CaW, carotid web; CTA, computed tomography angiography; DSA, digital subtraction angiography.

Representative imaging findings are shown in Figure 2. In typical cases, DSA demonstrated a shelf-like protrusion originating from the posterior wall of the internal carotid artery bulb, characteristic of CaW (Figure 2A). In some cases, there was persistent contrast retention over the web surface during middle and late contrast phases, indicating altered hemodynamics (Figure 2B,2C). Notably, in Case 16, DSA showed occlusion of both the A3 segment of the anterior cerebral artery and the M2 segment of the middle cerebral artery, which was successfully recanalized using stent retrieval (Figure 2D-2F).

Figure 2 DSA imaging of case 16. (A) DSA reveals a shelf-like protrusion at the origin of the right internal carotid artery in the early contrast phase (red arrow). (B,C) DSA demonstrates contrast retention over the web surface during the middle and late contrast phases (red arrow). (D) DSA shows occlusion of the A3 segment of the right anterior cerebral artery (blue arrow). (E) Selective microcatheter angiography reveals occlusion in the M2 segment of the MCA (blue arrow). (F) Successful recanalization of the M2 segment of the right MCA after stent retrieval. DSA, digital subtraction angiography; MCA, middle cerebral artery.

Further insights into the morphology of CaW were obtained in one patient who underwent CEA. Comprehensive ultrasound and histopathological evaluation provided further insights into the characteristics of CaW. Doppler ultrasound revealed thrombus formation and a thin intimal projection into the right carotid bifurcation (Figure 3A). Gross examination after carotid CEA revealed a diaphragm-like structure with an adherent thrombus (Figure 3B). Notably, no evidence of focal dissection was observed. Histopathological analysis using hematoxylin and eosin (H&E) staining confirmed significant fibromuscular proliferation and the presence of mixed thrombi within the excised web (Figure 3C,3D).

Figure 3 Ultrasound, gross specimen, and histopathological findings of the carotid web in Case 16. (A) Doppler ultrasound shows a blood clot (red arrow) and a thin tissue projection (blue arrow) into the right carotid bifurcation. (B) Gross specimen after CEA reveals a diaphragm-like structure (blue arrow) with an adherent thrombus (red arrow). (C) H&E staining shows significant fibromuscular proliferation within the carotid web. Scale bar, 100 µm. (D) H&E staining confirms that the attached thrombus is a mixed thrombus. Scale bar, 100 µm. CEA, carotid endarterectomy; H&E, hematoxylin and eosin.

The main characteristics of patients with or without symptomatic CaW are presented in Table 1. Univariate analysis showed that the median age of the CaW+ group was significantly lower than that of the CaW− group [53 (IQR, 46–58) vs. 65 (IQR, 56–72) years; P<0.001]. The proportion of males in the CaW+ group was lower compared to the CaW− group, although this difference did not reach statistical significance (56.3% in CaW+ vs. 62.9% in CaW−; P=0.593). The prevalence of previous ischemic stroke, hypertension, diabetes mellitus, and smoking history did not significantly differ between the CaW+ and CaW− groups. Notably, none of the CaW+ patients had atrial fibrillation, compared to 47.0% of the CaW− patients (P<0.001). There was a significant difference in the distribution of occlusion sites between the two groups. The CaW+ group had fewer occlusions in the intracranial internal carotid artery (6.3% vs. 40.0%; P=0.014) and more occlusions in the first segment of the middle cerebral artery (81.3% vs. 54.0%; P=0.032). Successful recanalization (mTICI 2b–3) was achieved in 93.8% of patients in the CaW group and 76.1% in the CaW− group; however, this difference was not statistically significant (P=0.133). The rate of symptomatic intracranial hemorrhage (ICH) was comparable between groups (6.3% vs. 7.0%, P>0.99). After 90 days, a favorable functional outcome (mRS 0–2) was observed in 93.8% (15/16) of patients with CaW, compared to 45.7% (176/385) of patients without CaW, with statistical significance (P<0.001).

After adjusting for potential confounders including age, occlusion site, and recanalization status, multivariable logistic regression analysis showed that the presence of CaW remained independently associated with a favorable 90-day outcome [odds ratio (OR) =9.70, 95% CI: 1.15–82.02, P=0.037]. In addition, younger age (OR =0.96, 95% CI: 0.94–0.98, P<0.001), proximal occlusion site (OR =1.78, 95% CI: 1.13–2.78, P=0.012), and successful recanalization (OR =5.84, 95% CI: 3.19–10.70, P<0.001) were also independently associated with favorable outcomes. These findings suggest that CaW may be a favorable prognostic marker in patients with anterior-circulation LVO undergoing thrombectomy (Table 2).

The characteristics of all patients with CaW are detailed in Table 3. To prevent stroke recurrence, 10 (62.5%) patients received antiplatelet therapy, 4 (25.0%) underwent carotid artery stenting (CAS), and 2 (12.5%) underwent CEA. During the follow-up period (median 29 months, range 5–70), patients 2 and 9, who initially received antiplatelet therapy, experienced recurrent ipsilateral strokes at 10 and 18 months, respectively, and subsequently underwent CEA and CAS.

Discussion

Our study is the first and largest investigation to estimate the prevalence of acute anterior circulation LVO associated with CaW in an Asian Han population. We observed that 3.99% of patients with acute ischemic stroke due to anterior circulation LVO presented with a symptomatic CaW at the carotid bifurcation. CaW was more commonly found in younger patients, with no significant gender difference. Intracranial LVO caused by CaW tends to involve the M1 segment of the middle cerebral artery. Patients with CaW-related anterior circulation LVO who underwent mechanical thrombectomy demonstrated favorable functional outcomes.

The prevalence of CaW in the general population remains unknown. In an unselected, continuous ischemic stroke population, the prevalence of CaW is 1.2%, with 0.7% occurring ipsilaterally to the stroke (14). Studies indicate a higher incidence of CaW in patients with anterior circulation intracranial LVO (8,15). However, due to selection biases such as race and inclusion criteria, the reported prevalence of CaW in patients with intracranial LVO varies widely, ranging from 0.7% to 13.5% (5-8). A retrospective cohort study from a single center in France, predominantly involving African American patients, reported that 11 out of 1,430 patients (0.7%) with acute LVO undergoing endovascular treatment had ipsilateral CaW (6). However, this study included patients with posterior circulation stroke, which may underestimate the true prevalence of CaW. A multicenter retrospective study from France found a 13.5% prevalence of CaW in patients with acute anterior circulation LVO (8). This study included a small sample size and excluded patients older than 65 years, potentially overestimating the prevalence of CaW in anterior circulation LVO. An analysis of the MR CLEAN trial—a multicenter randomized clinical trial of endovascular treatment for acute ischemic stroke in the Netherlands—revealed a prevalence of symptomatic CaW of 2.5% among patients with intracranial LVO (7), which is relatively close to our findings. One possible reason for the relatively high prevalence of CaW observed in our study is that we excluded anterior-circulation LVO patients who received intravenous thrombolysis alone or were managed conservatively owing to mild symptoms, and therefore did not undergo mechanical thrombectomy. Notably, our study identified a small contralateral protrusion in only 1 of the 16 patients with CaW, a prevalence considerably lower than the previously reported range of 30–60% (7,16). This discrepancy may partly reflect the inconsistent application of CTA in our cohort, given its higher sensitivity for detecting CaW (16).

Current research on CaW predominantly focuses on African American populations (4,9,17). CaW is frequently identified in younger ischemic stroke patients, with a systematic literature review revealing a median age of 46 years among patients with symptomatic CaW-associated ischemic stroke (17). A meta-analysis indicated that the overall prevalence of ipsilateral CaW in patients younger than 60 with cryptogenic stroke is 13% (18). However, large sample studies from Asian populations are lacking. A study from Japan reported a median age of 55 years (IQR, 48–65 years) among suspected stroke patients with CaW (10), which is comparable to our findings.

Classic FMD exhibits a female predominance, with women accounting for approximately 91% of cases (19). However, the proportion of females reported in cases of symptomatic CaW is lower than in classic FMD, though females still constitute the majority. In a systematic review describing 158 acute ischemic stroke patients with symptomatic CaW, 67% were female (17). In various case series comprising 50 patients with symptomatic CaW-related LVO, 66% were female (5,6,20). In contrast, our study population had a relatively higher proportion of males (56%), which aligns with the male predominance observed in intimal-type renal FMD patients (21).

The etiology of stroke may influence the prognosis of patients with LVO undergoing endovascular treatment (22,23). Currently, data on the prognosis of patients with symptomatic CaW-related LVO undergoing endovascular treatment are limited. A case series involving 11 patients with symptomatic CaW-related LVO reported that 10 patients (91%) achieved a good functional outcome (mRS 0–2) at 3 months post-endovascular treatment (6). Another study assessing stroke recurrence in patients with CaW found that, over a 2-year follow-up period, 24 out of 29 patients (83%) with symptomatic CaW-related LVO attained excellent functional outcomes (mRS 0–1) (20). Our study further corroborates these findings, demonstrating that patients with CaW-related LVO have significantly favorable outcomes following endovascular treatment. A possible explanation is that patients in the CaW+ group tended to be younger, and emboli from artery-to-artery embolism were likely smaller (16), contributing to the higher recanalization rate observed after endovascular treatment in this group.

Secondary prevention strategies for symptomatic CaW remain unestablished. Observational data suggest that despite medical therapy, symptomatic CaW patients may face up to a 20% risk of stroke recurrence within two years (20,24). Additionally, a systematic review reported that 56% (25 out of 45) of patients with symptomatic CaW experienced stroke recurrence within one year of follow-up (17). Small-scale studies have shown that CAS or CEA may be safe and effective treatment options for patients with symptomatic CaW (17,25,26). In our cohort, 2 out of 10 patients who received medical therapy experienced stroke recurrence over a median follow-up period of 29 months, suggesting that medical therapy alone may not provide sufficient protection for patients with CaW. CAS and CEA have been shown to be effective therapeutic strategies (4,9,16). However, in our cohort, only four patients underwent CAS and two underwent CEA, largely due to family concerns regarding financial burdens and perceived procedural risks.

Limitations

Our study has several limitations. First, while this is the largest investigation of symptomatic CaW in an Asian Han population to date, the sample size of CaW patients was relatively small (n=16), which limits the statistical power to detect subtle differences and associations. This small cohort may also reduce the generalizability of the findings, especially when comparing the outcomes with larger studies from different populations. Second, the study was conducted at two stroke centers in China, which may further limit the external validity and applicability of these results to other healthcare settings or populations, including different Asian subgroups and ethnicities. Future multicenter studies with more diverse populations are needed to verify these findings. Third, although CaW was diagnosed using DSA as the gold standard, supported by other imaging techniques like Doppler ultrasound, CTA, and MRA, the diagnosis of CaW remains challenging. Discrepancies in imaging interpretation and the subtle nature of CaW can lead to potential misclassification, which might have impacted the results. A standardized diagnostic protocol may help mitigate this issue in future studies.

Conclusions

In this study, we observed that CaW is more frequently identified in younger patients with anterior circulation LVO, particularly affecting the M1 segment of the middle cerebral artery. Patients with CaW-related LVO who underwent mechanical thrombectomy showed significantly favorable functional outcomes. Further larger studies are necessary to validate these findings and to investigate optimal prevention strategies for stroke recurrence.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-24-2426/rc

Data Sharing Statement: Available at https://qims.amegroups.com/article/view/10.21037/qims-24-2426/dss

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-24-2426/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 and its subsequent amendments. This study was deemed exempt by the ethics committee’s board for a formal IRB request, and individual consent for this retrospective analysis was waived.

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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