Assessment of association between the carotid web and dissection in spontaneous internal carotid artery dissection patients using vessel wall MRI

Abstract

Background

Internal carotid artery dissection (ICAD) is the major cause of ischemic stroke in young to middle-aged people. Recognition of predisposing factors may facilitate in early individual risk prediction and expand treatment.

Purpose

To evaluate the association between a carotid web and dissection in patients with ICAD using vessel wall magnetic resonance imaging (VW-MRI).

Material and Methods

A retrospective study was conducted of 223 patients who underwent VW-MRI. Of these patients, 58 patients with craniocervical artery dissection (CCAD) (33 ICAD and 25 vertebrobasilar artery dissection [VBAD]) were included. The control group (n = 165) consisted of patients without arterial dissection who had undergone VW-MRI . The presence of a carotid web in the posterior aspect of carotid bulb was recorded. The distance between the carotid web and start of dissection in ICA was recorded.

Results

The presence of a carotid web showed a significant difference between the ICAD, VBAD, and control groups (19 [57.6%] vs. 5 [20%] vs. 36 [21.8%], respectively; P < 0.001). In multi-nominal analysis, the presence of a carotid web showed a significant difference between the ICAD and VBAD groups and the ICAD and control groups (P < 0.05), with odds ratios of 5.41 (95% confidence interval [CI]=1.634–17.973) and 4.81 (95% CI=2.176–10.651), respectively. Out of 19 ICAD patients with carotid web, 16 had occurrence of dissection in the C1 segment of the ICA with a mean distance of 1.91 ± 1.71 cm from the carotid web.

Conclusion

Presence of a carotid web was more frequent in patients with ICAD. The carotid web may be one of the predisposing factors for development of dissection in patients with ICAD.

Keywords

Dissection vessel wall magnetic resonance imaging carotid web predisposing factor

Introduction

Dissection of the internal carotid artery (ICA) or vertebral artery is a common cause of cerebrovascular disease after atherosclerosis (1,2). It accounts for about 20%–25% of all ischemic stroke among young to middle-aged people (3,4). The cause of internal carotid artery dissection (ICAD) is considered to be either traumatic or spontaneous in origin (5). A large number of patients with spontaneous dissection are idiopathic. Any factors leading to vessel wall weakness is thought to be the cause of spontaneous dissection (6). Some studies have shown that underlying pathologies such as fibromuscular dysplasia, atherosclerosis, Marfan syndrome, osteogenesis imperfecta type I, Ehlers-Danlos syndrome type IV, recent infection, and migraine are associated with an increased risk of spontaneous dissection (1,6,7). However, these arteriopathies have been identified in only about 5%–15% of patients with spontaneous dissection (5,8,9).

A carotid web is defined as a membrane-like thin shelf of tissue usually located at the origin (posterior aspect) of the ICA (10,11). A recent study described the flow pattern in the lumen of carotid bulb using computational fluid dynamics and has found that the carotid web was associated with large surface of recirculated blood flow and higher wall shear stress (12). However, the association between the carotid web and dissection in patients with spontaneous ICAD has not been evaluated until now.

Digital subtraction angiography (DSA) has been the “gold standard” imaging modality for the detection of a carotid web due to its greater spatial resolution and contrast in vascular evaluation (13,14). However, due to high cost and invasiveness, several studies have recommended computed tomography angiography (CTA) as the choice of non-invasive imaging modality for the detection of a carotid web (10,14,15). Recently, vessel wall magnetic resonance imaging (VW-MRI) has been evolving in the assessment of craniocervical arteries (16,17). With the use of VW-MRI, the definitive diagnosis of arterial dissection has been improved (18). A recent study has demonstrated that VW-MRI is a definitive method in detecting a carotid web as it is dominant in providing accurate visual clues of carotid web morphology and location (19).

Thus, the aim of the present study was to evaluate the association between the carotid web and dissection in patients with spontaneous ICAD using VW-MRI.

Material and Methods

Participants

This retrospective study was approved by the institutional review board (IRB) of our hospital. Ethical approval was waived by the local Ethics Committee of Kunming Medical University given the retrospective nature of the study and all the procedures were performed as part of routine care.

The study comprised 223 consecutive patients (125 men [56.1%], 98 women [43.9%]; mean age = 50.10 ± 13.62 years) who underwent VW-MRI examination and enrolled in the study from March 2018 to January 2021. The indication for undergoing VW-MRI in our hospital was suspicion of various vascular diseases (such as atherosclerotic disease, arterial dissection, Moyamoya disease, vasculitis, reversible cerebral vasoconstriction syndrome, intracranial aneurysm) and carotid web by other imaging techniques (such as CTA and MRI). The diagnosis of arterial dissection was confirmed by two neuroradiologists (with 20 and 8 years of experience, respectively) based on characteristic radiological features of dissection (such as intramural hematoma [IMH], double lumen, and intimal flap) on VW-MRI (3). The final decision was achieved by consensus. Because spontaneous dissection is multifactorial and ICAD and vertebrobasilar artery dissection (VBAD) have the same arteriopathies as dissection, patients with VBAD were taken as one separate group for comparison. Patients with craniocervical artery dissection (CCAD) accompanied with arteriosclerosis and vasculitis were excluded as these vascular entities may be predisposing factors for the development of dissection. VW-MRI was performed within 10 days of the onset of clinical presentation. A total of 75 patients were diagnosed with CCAD but 17 were excluded from the study (14 patients had arteriosclerosis and three had vasculitis). Therefore, a total of 58 patients with CCAD were included in this study, comprising 33 patients with ICAD and 25 with VBAD. The control group participants were recruited from patients without arterial dissection who had undergone VW-MRI examination. A total of 165 patients were included in the control group (Fig. 1). Among 33 patients with ICAD, 10 patients had follow-up VW-MRI examinations for a duration of six months to 2 years. Among these follow-up patients, eight were ICAD patients with carotid web, and persistence of a carotid web was present.

Fig. 1.

Flow chart of participants in the study.

Demographic data such as sex, age, and risk factors such as hypertension, hyperlipidemia, and body mass index (BMI) were recorded for each patient. Written informed consent was obtained from all patients in the study.

MRI protocol

All patients with suspected CCAD underwent MRI examination using a 3.0-T MR scanner (Discovery MR750w; GE Healthcare, Milwaukee, WI, USA). The MRI protocol for these patients included VW-MRI (plain and contrast-enhanced [CE]-3D CUBE T1-weighted [T1W] image), high-resolution (HR) T2-weighted [T2W] image and carotid artery CE-magnetic resonance angiography (MRA). The parameters were as follows: HR T2W: TR/TE = 2179/80 ms, field of view (FOV) = 16 cm, matrix = 256 × 256, slice thickness = 2 mm, spacing = 0 mm, echo of length = 10, number of excitations (NEX) = 4, acquisition time = 3 min 51 s; 3D-T1 CUBE: TR/TE = 460/15 ms, FOV = 18 cm, matrix = 256 × 256, slice thickness = 0.8 mm, echo of length = 20, NEX = 2, acquisition time = 9 min 57 s; and CE-MRA: TR/TE = 4.5/1.4 ms, FOV = 28 cm, matrix = 320 × 256, slice thickness = 1.8 mm, echo of length = 10, NEX = 1, multi-phase = 2, acquisition time = 1 min 23 s. Post-contrast was performed 5 min after the injection of a single dose (0.1 mmol per kg of bodyweight) gadolinium-based contrast agent.

Image analysis

Image analysis was performed on a picture archiving and communication system (PACS) workstation by two experienced neuroradiologists (20 and 8 years of experience, respectively) and the final decision was achieved by consensus. The presence of a carotid web in each of the posterior wall of carotid bulb was recorded. Choi et al.’s definition of a carotid web on CTA, which is widely used, is “a thin intraluminal filling defect along the posterior wall of the carotid bulb just beyond the carotid bifurcation on oblique sagittal images and seen as a septum on axial images” (20). As VW-MRI provides an accurate visualization of the location and morphology of the carotid web (19), in our study, a carotid web was considered if the above characteristic imaging features were established on VW-MRI (Fig. 2). In addition, on contrast-enhanced imaging sequence, a carotid web shows slight enhancement and can be seen more clearly (21). The distance between the carotid web and start of dissection in the ICA was measured and recorded.

Fig. 2.

Bilateral carotid web in a normal patient. (a, c) CUBE T1W image shows protrusion along posterior wall of carotid bulb (b) with corresponding “thin septum” dividing the lumen. (d–f) CE CUBE T1W image shows clear carotid web with slight enhancement. (g–j) Note that the carotid web is not visible on MIP and thin slice CE-MRA images. CE, contrast-enhanced; MIP, maximum intensity projection; MRA, magnetic resonance angiography; T1W, T1-weighted.

Statistical analysis

To analyze data distribution, a normal probability test was carried out. All continuous variables with normal distribution were described as mean ± standard deviation (SD) and categorical variables were expressed as n (%). Between the three groups, continuous variables were compared using an analysis of variance (ANOVA) test, whereas categorical variables were compared using a chi-square test. If P ≤ 0.1 on the above analysis, variables were enrolled into multivariate analysis. Individual comparisons between the ICAD, VBAD, and control groups were performed with multinominal logistic regression analysis. With the enter stepwise method, multivariate logistic regression analysis was done to determine independent predictors of the ICAD. A value of P < 0.05 was considered to be statistically significant and all P values were two-sided. Statistical analysis was performed with SPSS version 25.0 (IBM Corp., Armonk, NY, USA).

Results

A total of 223 participants (125 men [56.1%], 98 women [43.9%]; mean age = 50.10 ± 13.62 years) were included in the study. The baseline demographics, risk factors, and presence of a carotid web between the ICAD, VABD, and control groups were compared in Table 1. The mean age of patients in the control group was significantly high compared to patients in the ICAD and VBAD groups (51.70 ± 13.14 years vs. 45.85 ± 12.39 years vs. 45.12 ± 16.91 years, respectively; P = 0.011). Sex, BMI, and risk factors (hypertension, hyperlipidemia) were not statistically significant between the ICAD, VBAD, and control groups. The presence of a carotid web in the ICAD group was significantly high compared to patients in the VBAD and control groups (19 [57.6%] vs. 5 [20%] vs. 36 [21.8%], respectively; P < 0.001).

Table 1.

Comparison of patient demographics, clinical data, and presence of carotid web between the ICAD, VBAD, and control groups.

	ICAD (n = 33)	VBAD (n = 25)	Control (n = 165)	P value
Age (years)	45.85 ± 12.39	45.12 ± 16.91	51.70 ± 13.14	0.011*
Male sex	21 (63.6)	14 (56.0)	90 (54.5)	0.630
BMI (kg/m²)	23.87 ± 24.9	22.83 ± 3.47	23.61 ± 3.39	0.457
Risk factors
Hypertension	10 (30.3)	9 (36.0)	63 (38.2)	0.690
Hyperlipidemia	5 (15.2)	2 (8.0)	19 (11.5)	0.698
Carotid web	19 (57.6)	5 (20.0)	36 (21.8)	<0.001*

Values are given as n (%) or mean ± SD.

*P < 0.05.

BMI, body mass index; ICAD, internal carotid artery dissection; VBAD, vertebrobasilar artery dissection.

In multi-nominal analysis, there was no difference in age between the ICAD and VBAD groups. There was a significant difference in age between the ICAD and control groups and the VBAD and control groups (P < 0.05). There was a significant difference in the presence of a carotid web between the ICAD and VBAD groups and the ICAD and control groups in the multi-nominal analysis (P < 0.05), with odds ratios (OR) of 5.41 (95% confidence interval [CI] = 1.634–17.973) and 4.81 (95% CI = 2.176–10.651), respectively (Table 2). There was no significant difference in the presence of a carotid web between the VBAD and control groups in the multi-nominal analysis.

Table 2.

Multi-nominal logistic analysis of age and presence of carotid web between ICAD vs VBAD, ICAD vs. control group, and VBAD vs control group.

Groups		OR	95% CI	P value
ICAD vs. VBAD	Age	0.997	0.957–1.039	0.887
ICAD vs. VBAD	Carotid web	5.419	1.634–17.973	0.006*
ICAD vs. control	Age	1.034	1.003–1.066	0.034*
ICAD vs. control	Carotid web	4.814	2.176–10.651	<0.001*
VBAD vs. control	Age	0.964	0.934–0.996	0.026*
VBAD vs. control	Carotid web	1.125	0.391–3.236	0.827

*P < 0.05.

ICAD, internal carotid artery dissection; VBAD, vertebrobasilar artery dissection.

Out of 19 ICAD patients with carotid web, 16 had dissection in the C1 segment of the ICA with a mean distance of 1.91 ± 1.71 cm (distance between the carotid web and start of dissection) (Figs. 3 and 4). Three ICAD patients with carotid web, had dissection in the C2, C4, and C6 segments of the ICA.

Fig. 3.

Carotid web in a patient with ICAD. (a) CUBE T1W image shows protrusion along the posterior wall of the carotid bulb (yellow arrow) and hyperintense IMH in the right C1 segment of the ICA (green arrow). Note that the start of dissection is near the carotid web. (b, c) Plain and CE axial CUBE T1W image shows corresponding “thin septum” dividing the lumen. (d) CE CUBE T1W image shows slight enhancement in the carotid web. (e–g)Note that the carotid web is not visible on MIP and thin slice CE-MRA images. (h–k) Follow-up after two years: plain and CE CUBE T1W image shows persistence of carotid web (yellow arrow) with resolve IMH. CE, contrast-enhanced; ICA, internal carotid artery; ICAD, internal carotid artery dissection; IMH, intramural hematoma; MIP, maximum intensity projection; T1W, T1-weighted.

Fig. 4.

Occurrence of dissection close to carotid web. (a) CUBE T1W image shows protrusion along the posterior wall of the carotid bulb and hyperintense IMH in the left C1 segment of the ICA. Note that the start of dissection is near the carotid web (yellow arrow). (b, c) Plain and CE axial CUBE T1W image shows corresponding “thin septum” dividing the lumen. (d) CE CUBE T1W image shows slight enhancement in carotid web. (e) Subtraction image of plain and CE CUBE T1W image shows clear close distance between the carotid web and the start of the dissection (intimal flap) (yellow arrow), (f) with corresponding “thin septum” of the carotid web with contrast enhancement. (g,h) Note that carotid web is not visible on thin slice CE-MRA images. CE, contrast-enhanced; ICA, internal carotid artery; IMH, intramural hematoma; MRA, magnetic resonance angiography; T1W, T1-weighted.

Discussion

The present study showed a higher prevalence of carotid web in patients with spontaneous ICAD compared to the VBAD and control groups. Furthermore, we found that most of the patients with ICAD with a carotid web had dissection in the C1 segment of the ICA and the mean distance from the carotid web to the start of dissection was 1.91 ± 1.71 cm.

In 1968, Rainer et al. first reported a carotid web as the cause of recurrent transient neurological symptoms in a young female patient (22,23). Since then, many studies have demonstrated the association of a carotid web with cryptogenic stroke and the occurrence of recurrent ischemic stroke (10,11,15,24,25). The association of a carotid web and development of dissection has not been evaluated until now. The pathogenesis of the carotid web has not been clear until now, but most previous studies considered a carotid web to be developmental in origin (14). Histopathological examination of resected carotid web specimens has revealed features such as abnormal intimal fibrosis and smooth muscle cell hyperplasia (26). Previous studies have used DSA and CTA as imaging modalities in series of carotid webs (11,13,20,27). Even though DSA has higher temporal and spatial resolution, the risk of misdiagnosing a carotid web may be present when only two standard projections (frontal and lateral) are obtained, since the carotid web is located on the posterior wall of the ICA (13,24). Compared to CTA, VW-MRI not only has the ability to provide hemodynamic information, but it can also provide more information about the arterial wall and lesions as well as help differentiate and diagnose from other diseases such as atherosclerotic plaques and arterial dissection (19,28). In addition, MRI has the advantage of imparting no radiation (19).

VW-MRI has an added aspect when diagnosing arterial dissection, as it contributes direct visualization and characterization of the wall of the vessel (17,19,29 –32). A study conducted on arterial dissection found an intimal flap on luminal imaging (CTA, MRA, or DSA) in 16% of patients while on VW-MRI it was found in 42% (33). Similarly, another study demonstrated that with the use of VW-MRI, compared to time-of-flight MRA alone, the diagnosis rate of intracranial dissection was improved from 11% to 22% (18).

Compagne et al. demonstrated that a carotid web is associated with increased recirculation area and increased transverse wall shear stress (12), and Osswald et al. suggested that an increase in wall shear stress is one of the risk factors for the development of dissection (34). In this study, using VW-MRI we observed that presence of a carotid web was more likely to be found in patients with spontaneous ICAD compared to the VBAD and control groups (57.6% vs. 20% vs. 21.8%; P < 0.001). In multi-nominal analysis, the presence of a carotid web showed a strong correlation with patients with ICAD (ICAD vs. VBAD: OR = 5.41; ICAD vs. control: OR = 4.81; P < 0.05). We also observed that 16 out of 19 ICAD patients with carotid web had dissection in the C1 segment of the ICA with a mean distance of 1.91 ± 1.71 cm from the carotid web. Our findings not only correlate with previous studies (12,34), but also provide stronger evidence, with occurrence of dissection at a closer distance to the carotid web.

Limited data are available about the prevalence of a carotid web in the general population. Previous studies have shown a prevalence of 1%–1.2% of carotid web in patients with suspected ischemic stroke who underwent CTA (11,20). Recent studies have shown a prevalence of 9.4%–23% of carotid web in patients with ischemic stroke and 1%–7% in non-stroke patients (27,35). In our study, there were 60 patients with a carotid web among 223 patients (26.9%). The prevalence of a carotid web was 57.6% in patients with ICAD, 20% in patients with VBAD, and 21.8% in the control group. The prevalence of a carotid web is higher in our study compared to previous studies. Previous studies used CTA as the imaging technique, whereas VW-MRI was the technique of choice in our study for the detection of a carotid web. Although the carotid web has characteristic imaging features, it could be missed or misinterpreted as atherosclerotic plaque or dissection (25). To avoid misinterpretation in our study, we used plain and contrast-enhanced HR VW-MRI as the imaging technique for the detection of a carotid web. Furthermore, some patients had follow-up VW-MRI examinations to see if there were significant changes in the carotid web to rule out the possibility of atherosclerotic plaque.

The present study has some limitations. First, the sample size of dissection patients was small in this study, as the annual incidence of patients with symptomatic spontaneous CCAD is 2.5–3 per 100,000 (8). Second, the study was based on single center so there might be a potential selection bias in our study. Third, the diagnosis of carotid web was confirmed primarily based upon VW-MRI without histopathological examination. However, previous studies have reported that an imaging-based diagnosis is a sensitive method for the diagnosis of carotid web and VW-MRI is a reliable method in the detection of a carotid web (19). Finally, this is a cross-sectional study, and further longitudinal studies are needed to evaluate patients with and without a carotid web for the occurrence of dissection and validate the findings in our study.

In conclusion, we found the presence of a carotid web was more frequent in patients with ICAD. A carotid web may be one of the predisposing factors for the development of dissection in the ICA. This finding in our study may help us better understand the underlying pathogenesis of ICAD.

Footnotes

Acknowledgements

The authors thank and appreciate the contribution of all the investigators (Chao Gao, Yizhen Zeng, Kaipeng Xie, Yixin Shi, and Lei Zhao) in the study.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

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 the Yunnan Provincial Science and Technology Department & Kunming Medical University Applied Basic Research (grant number 2019FE001 (-052)).

ORCID iD

Zongfang Li

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