Association of circumferential aneurysm wall enhancement with recurrence after coiling of unruptured intracranial aneurysms: a preliminary vessel wall imaging study

Takeshi Hara Department of Neurosurgery and Interventional Neuroradiology, Hiroshima City Asa Citizens Hospital; and

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Toshinori Matsushige Department of Neurosurgery and Interventional Neuroradiology, Hiroshima City Asa Citizens Hospital; and

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Michitsura Yoshiyama Department of Neurosurgery and Interventional Neuroradiology, Hiroshima City Asa Citizens Hospital; and

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Yukishige Hashimoto Department of Neurosurgery and Interventional Neuroradiology, Hiroshima City Asa Citizens Hospital; and

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Shohei Kobayashi Department of Neurosurgery and Interventional Neuroradiology, Hiroshima City Asa Citizens Hospital; and

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Shigeyuki Sakamoto Department of Neurosurgery, Graduate School of Biomedical and Health Sciences, Hiroshima University, Hiroshima, Japan

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OBJECTIVE

Recent histopathological studies of unruptured intracranial aneurysms (UIAs) have confirmed that aneurysm wall enhancement (AWE) on MR vessel wall imaging (VWI) is related to wall degeneration with in vivo inflammatory cell infiltration. Therefore, pretreatment aneurysm wall status on VWI may be associated with recurrence after endovascular treatment.

METHODS

VWI with gadolinium was performed on 67 consecutive saccular UIAs before endovascular treatment between April 2017 and June 2021. The mean (range) follow-up period after treatment was 24.4 (6–54) months. AWE patterns were classified as circumferential AWE (CAWE), focal AWE (FAWE), and negative AWE (NAWE). The authors retrospectively investigated the relationship between aneurysm recurrence and AWE patterns, as well as conventional risk factors.

RESULTS

Sixty-seven patients with 67 saccular UIAs were eligible for the present study. AWE patterns were as follows: 10 CAWE (14.9%), 20 FAWE (29.9%), and 37 NAWE (55.2%). Follow-up MRA detected aneurysm recurrence in 18 of 69 cases (26.1%). Univariate analysis identified maximum diameter (mean ± SD 5.8 ± 2.2 mm in patients with stable aneurysms vs 7.7 ± 3.8 mm in those with unstable aneurysms, p = 0.02), aspect ratio (1.4 ± 0.5 vs 1.1 ± 0.4, p < 0.01), aneurysm location in posterior circulation (4.1% vs 27.8%, p < 0.01), volume embolization ratio (29.6% ± 7.8% vs 25.2% ± 6.1%, p = 0.02), and AWE pattern (p = 0.04) as significant predictive factors of recurrence. Among the 3 AWE patterns, CAWE was significantly more frequent in the unstable group, but no significant differences in stability of the treated aneurysms were observed with the FAWE and NAWE patterns. In multivariate logistic regression analysis, CAWE pattern (OR 14.2, 95% CI 1.8–110.8, p = 0.01) and volume embolization ratio ≥ 25% (OR 8.6, 95% CI 2.1–34.3, p < 0.01) remained as significant factors associated with aneurysm stability after coiling.

CONCLUSIONS

VWI before coiling provides novel insights into the stability of treated aneurysms. Aneurysms with the CAWE pattern on VWI before coiling may be less stable after treatment.

ABBREVIATIONS

AWE = aneurysm wall enhancement; CAWE = circumferential AWE; FAWE = focal AWE; IA = intracranial aneurysm; MRRC = modified Raymond-Roy occlusion classification; NAWE = negative AWE; TOF = time-of-flight; UIA = unruptured IA; VER = volume embolization ratio; VWI = vessel wall imaging.

OBJECTIVE

Recent histopathological studies of unruptured intracranial aneurysms (UIAs) have confirmed that aneurysm wall enhancement (AWE) on MR vessel wall imaging (VWI) is related to wall degeneration with in vivo inflammatory cell infiltration. Therefore, pretreatment aneurysm wall status on VWI may be associated with recurrence after endovascular treatment.

METHODS

VWI with gadolinium was performed on 67 consecutive saccular UIAs before endovascular treatment between April 2017 and June 2021. The mean (range) follow-up period after treatment was 24.4 (6–54) months. AWE patterns were classified as circumferential AWE (CAWE), focal AWE (FAWE), and negative AWE (NAWE). The authors retrospectively investigated the relationship between aneurysm recurrence and AWE patterns, as well as conventional risk factors.

RESULTS

Sixty-seven patients with 67 saccular UIAs were eligible for the present study. AWE patterns were as follows: 10 CAWE (14.9%), 20 FAWE (29.9%), and 37 NAWE (55.2%). Follow-up MRA detected aneurysm recurrence in 18 of 69 cases (26.1%). Univariate analysis identified maximum diameter (mean ± SD 5.8 ± 2.2 mm in patients with stable aneurysms vs 7.7 ± 3.8 mm in those with unstable aneurysms, p = 0.02), aspect ratio (1.4 ± 0.5 vs 1.1 ± 0.4, p < 0.01), aneurysm location in posterior circulation (4.1% vs 27.8%, p < 0.01), volume embolization ratio (29.6% ± 7.8% vs 25.2% ± 6.1%, p = 0.02), and AWE pattern (p = 0.04) as significant predictive factors of recurrence. Among the 3 AWE patterns, CAWE was significantly more frequent in the unstable group, but no significant differences in stability of the treated aneurysms were observed with the FAWE and NAWE patterns. In multivariate logistic regression analysis, CAWE pattern (OR 14.2, 95% CI 1.8–110.8, p = 0.01) and volume embolization ratio ≥ 25% (OR 8.6, 95% CI 2.1–34.3, p < 0.01) remained as significant factors associated with aneurysm stability after coiling.

CONCLUSIONS

VWI before coiling provides novel insights into the stability of treated aneurysms. Aneurysms with the CAWE pattern on VWI before coiling may be less stable after treatment.

In Brief

It remains an interdisciplinary challenge to predict the status of coiled aneurysms. The circumferential aneurysm wall enhancement pattern on MR vessel wall imaging, which suggests a specific feature of aneurysm wall degeneration, may have a negative association with the durability of coiled aneurysms. The characteristics of unruptured intracranial aneurysms on vessel wall imaging before coiling may be novel predictors of aneurysm recurrence and may facilitate the selection of treatment options or endovascular treatment strategies.

Unruptured intracranial aneurysms (UIAs) affect approximately 5% of the population, and these patients may have subarachnoid hemorrhage.1 The prevalence of actual aneurysmal rupture is low, except for those greater than 7 mm; therefore, the long-term durability of treated aneurysms is expected. Due to significant advances in the endovascular treatment of intracranial aneurysms (IAs) as a result of technological innovations and the development of supportive devices, including coil materials, neck-bridging devices, flow-diverting stents, and intra-aneurysmal structures, endovascular treatment may be applied to UIAs. Recent studies reported that endovascular treatment improved postoperative quality of life of patients and had lower morbidity and mortality rates than microsurgical clipping.24 However, the long-term durability of endovascular treatment remains the primary concern. Follow-up of coiled aneurysms is crucial because recurrence and regrowth occur in approximately 10%–20% of treated aneurysms, even those treated with neck-bridging devices.5,6 MRI is one of the standard modalities used to evaluate treated aneurysms. MR vessel wall imaging (VWI) is increasingly used to identify intracranial vascular pathologies, such as atherosclerosis, dissection, vasculitis, and corresponding vessel wall inflammation.7,8 Previous studies suggested that age,9,10 aneurysmal size and neck width,1113 and the volume embolization ratio (VER)1416 were associated with recurrence after coiling, whereas specific histopathological features of recurrent IAs such as impairments in smooth muscle cells and in vivo infiltration of inflammatory cells17 were recently identified as contributing factors.

We hypothesized that VWI may be used to confirm whether the presence of these pathological characteristics before treatment is associated with instability after treatment. Therefore, herein we investigated the relationship between aneurysm wall enhancement (AWE) patterns on VWI before treatment and recurrence after coiling.

Methods

Study Population

Between April 2017 and June 2021, 222 consecutive patients harboring 298 saccular UIAs were prospectively evaluated with VWI. Seventy-two UIAs were treated with coil embolization and 73 with microsurgical clipping, whereas 153 were monitored as requested by patients. UIAs located in the cavernous portion of the internal carotid artery were excluded from the present study due to concerns regarding the reliability of exact evaluations of contrast enhancement in the surrounding cavernous sinus and adherent dura mater.

Patient Demographic and Aneurysm Characteristics

Patient demographic and aneurysm characteristics were retrospectively obtained from medical records. The following information was collected about patients: sex, age, comorbidities, and smoking status. The morphological characteristics of the aneurysms, including maximum size, location (anterior/posterior circulation), and aspect ratio (height divided by neck width), were evaluated with 3D digital subtraction angiography. Furthermore, the following factors associated with endovascular treatment were reviewed: VER, use of stents, and immediate embolization status according to the modified Raymond-Roy occlusion classification (MRRC).

Endovascular Procedures

Endovascular coil embolization was performed with the patient under general anesthesia. Bare platinum coils (Axium Prime [Medtronic], Target [Stryker], and ED [Kaneka Medix] coils) and bioactive coils (HydroCoil [MicroVention Terumo]) were used. Balloon-remodeling or stent-assisted techniques were selected on the basis of aneurysm neck morphology. An LVIS (MicroVention Terumo) or Neuroform (Stryker) stent was used for stent-assisted coiling. VER was calculated as the ratio of packed coil volume to aneurysm volume. Immediate embolization status was qualitatively classified as class I to IIIb according to MRRC.18 We also dichotomized aneurysms as class I–II and IIIa–IIIb to analyze the relationship of class with aneurysm recurrence.19

Imaging Protocol

All patients underwent scanning with a 1.5-T MR scanner (Signa Explorer, GE Healthcare Ltd.) equipped with an 8-channel head coil. The protocol included 3D time-of-flight (TOF) MRA for localization of subsequent scans and T1-weighted 3D black-blood fast spin echo with high-resolution MRI (CUBE) before and 3 minutes after administration of 0.1 mmol/kg Gd-BT-DO3A (Gadovist, Bayer Schering Pharma).

Image Analysis

MR VWI was performed before endovascular treatment. A radiologist and neurosurgeon evaluated for the presence of AWE by referring to noncontrast VWI and vessel anatomy shown with TOF MRA. The presence and location of contrast enhancement were qualitatively assessed on subtraction images obtained before and after contrast VWI in multiple planes. AWE was classified into the following 3 patterns, as previously reported:20 1) circumferential AWE (CAWE), i.e., wall enhancement in the broad part of the aneurysm wall; 2) focal AWE (FAWE), i.e., partial enhancement in the aneurysm wall; and 3) negative AWE (NAWE), i.e., no enhancement in the aneurysm wall. Representative cases of these patterns are shown in Fig. 1.

FIG. 1.
FIG. 1.

Representative cases of 3 AWE patterns evaluated with T1-weighted 3D black-blood fast spin echo MRI performed after contrast enhancement. A and B: CAWE and FAWE (arrows). C: No enhancement (arrowhead). The insets show the enhancement patterns.

Follow-Up Regimen

All patients were monitored with TOF MRA 6, 12, and 24 months after treatment and annually thereafter. The results of follow-up MRA were compared with those of MRA obtained 1 day after treatment as a reference. Aneurysms with any visually detected signal inside the coiled aneurysm or enlarged remnants of any size on TOF MRA were defined as unstable.

Statistical Analysis

Statistical analysis was performed with JMP statistical package version 14 (SAS Institute Inc.). AWE patterns were evaluated by 2 raters who were blinded to clinical data and treatment results, and interrater agreement was assessed to calculate the κ coefficient. Categorical variables are presented as numbers and percentages, and continuous variables as the mean ± SD.

The Fisher’s exact test was performed to analyze categorical variables where appropriate. The Mann-Whitney U-test was used for unpaired continuous variables. Differences were defined as significant at a probability level of p < 0.05. Multivariate logistic regression analysis was performed to identify factors independently associated with aneurysm instability after coiling, including putative risk factors for aneurysm recurrence after coiling (i.e., aneurysm maximum diameter, use of stents, VER, and AWE pattern).

Results

Patient and Aneurysm Characteristics

Sixty-seven patients with 67 saccular UIAs were included in the present study. Patient demographic, aneurysm morphological, and treatment data are shown in Table 1. The patients included 20 males and 47 females (mean age ± SD 67.6 ± 12.2 years). Sixty aneurysms were located in the anterior circulation and 7 in the posterior circulation. The mean ± SD (range) maximum size of the aneurysms was 6.3 ± 2.8 (3.3–20) mm.

TABLE 1.

Patient demographic, aneurysm morphological, and treatment data

CharacteristicValue
Patient factors
 Age, yrs67.6 ± 12.2
 Female47 (70.1)
 Hypertension40 (59.7)
 Smoker23 (34.3)
Aneurysm factors
 Max size, mm6.3 ± 2.8
 Neck width, mm4.1 ± 1.9
 Aspect ratio1.3 ± 0.5
 Location
  Anterior circulation60 (89.6)
  Posterior circulation7 (10.4)
Treatment factors
 VER, %28.4 ± 7.6
 Use of a stent22 (32.8)
 Embolization status, MRRC class
  I22 (32.8)
  II34 (50.7)
  IIIa4 (6.0)
  IIIb7 (10.4)
AWE pattern
 Circumferential10 (14.9)
 Focal20 (29.9)
 Negative37 (55.2)

Values are shown as number (%) or mean ± SD.

Radiographic Outcomes

Interrater agreement regarding the evaluations of the AWE patterns was good (κ = 0.72, 95% CI 0.58–0.87). After the final consensus reading, the AWE patterns on VWI before treatment were classified as follows: 10 CAWE (14.9%), 20 FAWE (29.9%), and 37 NAWE (55.2%). Follow-up MRA detected signal changes around the aneurysmal neck in 18 of 67 cases at the 6-month follow-up. Six aneurysms exhibited regrowth, whereas 12 showed major coil compaction. One patient was retreated with microsurgical clipping and 1 with coil embolization. The other 16 patients were carefully monitored with MRI at the outpatient clinic.

Treatment Factors

Twenty-two aneurysms (32.8%) were treated with a neck-bridging stent, and VER was 28.4% ± 7.6% (range 14.9%–52.7%). Immediate embolization status, qualitatively classified according to MRRC, was class I for 22 (32.8%) aneurysms, class II for 34 (50.7%), class IIIa for 4 (6.0%), and class IIIb for 7 (10.4%).

Overall Predictors of Recurrence After Coiling

A comparison of aneurysm status after endovascular treatment is shown in Table 2. Univariate analysis identified AWE patterns (4 [8.2%] CAWE/16 [32.7%] FAWE/29 [59.2%] NAWE aneurysms among those that were stable vs 6 [33.3%] CAWE/4 [22.2%] FAWE/8 [44.4%] NAWE aneurysms among those that were unstable, p = 0.04), maximum diameter (5.8 ± 2.2 vs 7.7 ± 3.8 mm, respectively; p = 0.02), aspect ratio (1.4 ± 0.5 vs 1.1 ± 0.4, p < 0.01), posterior circulation (4.1% vs 27.8%, p < 0.01), and VER (29.6% ± 7.8% vs 25.2% ± 6.1%, p = 0.02) as significant predictors of recurrence after coil embolization.

TABLE 2.

Univariate factors related to recurrence after coiling

CharacteristicStable (n = 49)Unstable (n = 18)p Value
Patient factors
 Age, yrs66.1 ± 12.971.5 ± 8.90.24
 Female37 (75.5)10 (55.6)0.11
 Hypertension33 (67.3)7 (38.9)0.04
 Smoker16 (32.7)7 (38.9)0.63
Aneurysm factors
 Max diameter, mm5.8 ± 2.27.7 ± 3.80.02
  ≥10 mm2 (4.1)2 (11.1)0.28
 Neck width, mm3.5 ± 1.25.6 ± 2.7<0.01
 Aspect ratio1.4 ± 0.51.1 ± 0.4<0.01
 Location<0.01
  Anterior circulation47 (95.9)13 (72.2)
  Posterior circulation2 (4.1)5 (27.8)
Treatment factors
 VER, %29.6 ± 7.825.2 ± 6.10.02
  ≥25%40 (81.6)8 (44.4)<0.01
 Use of a stent13 (26.5)9 (50.0)0.07
 Embolization status, MRRC class0.13
  I–II43 (87.8)13 (72.2)
  IIIa–IIIb6 (12.2)5 (27.8)
AWE pattern0.04
 Circumferential4 (8.2)6 (33.3)
 Focal16 (32.7)4 (22.2)
 Negative29 (59.2)8 (44.4)

Values are shown as number (%) or mean ± SD unless indicated otherwise. Boldface type indicates statistical significance (p < 0.05).

In multivariate logistic regression analysis, CAWE pattern (OR 14.2, 95% CI 1.8–110.8, p = 0.01) and VER ≥ 25% (OR 8.6, 95% CI 2.1–34.3, p < 0.01) remained as significant factors for aneurysm stability after coiling (Table 3).

TABLE 3.

Multivariate analysis of recurrence after coiling

VariableOR (95% CI)p Value
Max size ≥10 mm2.60 (0.15–45.57)0.512
Use of a stent2.12 (0.57–7.86)0.259
VER ≥25%8.57 (2.14–34.31)0.002
CAWE pattern14.21 (1.82–110.78)0.011

Boldface type indicates statistical significance (p < 0.05).

AWE Patterns and Aneurysm Recurrence After an Endovascular Approach

A subgroup analysis of the distribution of AWE patterns was conducted (Fig. 2). In the assessment of the AWE patterns in the unstable group, CAWE was significantly more frequent than FAWE (OR 6.00, 95% CI 1.13–31.99, p = 0.036) and NAWE (OR 5.43, 95% CI 1.23–24.07, p = 0.026). A representative case is shown in Fig. 3.

FIG. 2.
FIG. 2.

Distribution of AWE patterns in the unstable group. The CAWE pattern was significantly more frequent than the NAWE and FAWE patterns. *Significant at p < 0.05.

FIG. 3.
FIG. 3.

An unruptured 8.7-mm right internal carotid artery–posterior communicating artery aneurysm. Native (A) and contrast-enhanced (B) VWI performed before endovascular treatment showed CAWE (white arrowheads). The aneurysm was completely obliterated with a VER of 21.9% by using the Neuroform stent (black arrowhead) (C). Follow-up imaging performed 6 months after treatment showed recurrence at the neck segment (black arrowhead) (D).

Discussion

It remains an interdisciplinary challenge to predict the status of coiled aneurysms. Several factors have been identified as risk factors for the recurrence of aneurysms after coil embolization, including age9,10 as a patient factor, size and neck width1113 as well as aneurysm location13,21 as morphological factors, and VER,1416 use of stents,22,23 and degree of occlusion18,19 as treatment factors. The diagnostic value of the present study is that CAWE was associated with aneurysmal instability after coiling. VWI before coiling of IAs, which indicated histopathological features, may be a novel predictor of aneurysm recurrence and may facilitate the selection of treatment options or endovascular treatment strategies.

Previous studies reported the histopathological findings of coiled aneurysms in animal models.2428 Blood clots composed of red blood cells, fibrin, and inflammatory cells were generally present within the 1st week after aneurysm coiling, whereas inflammatory cell invasion occurred in the majority of patients after approximately 2 weeks and thereafter.24,27 After approximately 3 months, endothelial cells generally encroached along coils at the aneurysm neck. Two recent histological studies showed that the mechanism underlying IA recurrence involved impairments in smooth muscle cells and the infiltration of inflammatory cells.17,29 Furthermore, both H&E and CD68+ staining showed the presence of lymphocytes and macrophages in the walls of recurrent aneurysms, suggesting persistent chronic inflammation.29

Regarding the presence of AWE, the present study confirmed that presence of the CAWE pattern before coiling was associated with recurrence after coiling, as shown in Fig. 3. Previous studies on the relationship between VWI and the histopathology of UIAs showed that AWE was suggestive of atherosclerotic wall thickening with prominent wall inflammation and neovascularization.7,8 This may be a key finding indicative of aneurysm recurrence. Recent studies showed that AWE of UIAs was associated with aneurysm instability, as well as symptomatic growth and rupture.30,31 In the latest study, segmentation of AWE was explored. FAWE was associated with bleb formation, whereas CAWE was suggestive of whole sac expansion.20 FAWE potentially implies partial atherosclerosis with wall inflammation, however focal wall thickening may induce hemodynamic imbalance and damage the adjacent wall structure and thereby lead to bleb formation.32 On the contrary, most CAWE before coiling is suggestive of chronic inflammation throughout the aneurysm wall. Nevzati et al. recently reported that aneurysms with highly degenerated walls that were subjected to coil embolization were more prone to further wall degeneration, increased inflammation, and recanalization than those with normal walls.17 Even after coiling in the aneurysm sac, a prolonged wall inflammatory response may remain active. The potential range of wall degeneration before endovascular treatment may be a crucial factor. The latest study clarified the importance of the endothelial lining along the parental artery for the healing of coiled aneurysms.33 Prolonged inflammation in the aneurysm wall before endothelialization results in wall remodeling with increased wall vulnerability, insufficient thrombus organization, and failed neointima formation. We presumed that UIAs with CAWE may be at risk for regrowth after coiling and prolonged endothelialization. It would be of great interest to investigate if flow-diverting stents could serve as a scaffold for endothelialization and healing of UIAs with CAWE.

In the present study, the specific features of aneurysm recurrence were regrowth in 6 UIAs and compaction in 12. These 6 UIAs showed regrowth within 1 year of follow-up after coiling. When we examined the AWE patterns of the aneurysms with regrowth, 3 (50%) showed the CAWE pattern. Although this finding was not statistically significant in the present study, further research on regrowth is warranted. Moreover, the 12 UIAs that showed coil compaction may require close monitoring for potential regrowth.

Limitations

The present study included a small patient population treated at a single center. Therefore, we currently cannot reach a concrete conclusion regarding the clinical significance of the VWI findings before coiling and the clinical results. However, VWI may provide further insights into the healing of coiled aneurysms. Furthermore, histopathological verification was not performed in the present study. Although previous studies performed histopathological evaluations of recurrent aneurysms after coiling, it is technically challenging to harvest a portion of a coiled aneurysm when securing hemostasis with microsurgery.29 Moreover, because recurrence was evaluated within a relatively short period of 6 to 54 months, long-term stability after coiling remains unclear. Chronological changes in wall enhancement are also of interest. Based on the hypothesis that aneurysm wall degeneration may be a factor that contributes to aneurysm recurrence after coiling, consecutive VWI after coiling may provide novel insights into the healing process of treated aneurysms.

Conclusions

The CAWE pattern, which suggests a specific feature of aneurysm wall degeneration, may negatively affect the durability of coiled aneurysms. Although the long-term stability of coiled aneurysms and the requirement for retreatment currently remain unclear, VWI before coiling provides novel insights into the stability of coiled aneurysms.

Acknowledgments

We thank the MRI Team at Hiroshima City Asa Citizens Hospital for performing VWI.

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Matsushige, Hara, Hashimoto. Acquisition of data: Hara, Yoshiyama, Hashimoto, Kobayashi. Analysis and interpretation of data: Matsushige, Hara, Hashimoto. Drafting the article: Hara. Critically revising the article: Matsushige. Approved the final version of the manuscript on behalf of all authors: Matsushige. Statistical analysis: Hashimoto. Study supervision: Sakamoto.

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    Zhang X, Zuo Q, Tang H, et al. Stent assisted coiling versus non-stent assisted coiling for the management of ruptured intracranial aneurysms: a meta-analysis and systematic review. J Neurointerv Surg. 2019;11(5):489496.

    • Crossref
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  • 24

    Bavinzski G, Talazoglu V, Killer M, et al. Gross and microscopic histopathological findings in aneurysms of the human brain treated with Guglielmi detachable coils. J Neurosurg. 1999;91(2):284293.

    • Crossref
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  • 25

    Brinjikji W, Kallmes DF, Kadirvel R. Mechanisms of healing in coiled intracranial aneurysms: a review of the literature. AJNR Am J Neuroradiol. 2015;36(7):12161222.

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  • 26

    Dai D, Ding YH, Danielson MA, et al. Histopathologic and immunohistochemical comparison of human, rabbit, and swine aneurysms embolized with platinum coils. AJNR Am J Neuroradiol. 2005;26(10):25602568.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Groden C, Hagel C, Delling G, Zeumer H. Histological findings in ruptured aneurysms treated with GDCs: six examples at varying times after treatment. AJNR Am J Neuroradiol. 2003;24(4):579584.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Szikora I, Seifert P, Hanzely Z, et al. Histopathologic evaluation of aneurysms treated with Guglielmi detachable coils or matrix detachable microcoils. AJNR Am J Neuroradiol. 2006;27(2):283288.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Wang C, Li M, Chen H, Yang X, Zhang Y, Zhang D. Histopathological analysis of in vivo specimens of recurrent aneurysms after coil embolization. J Neurointerv Surg. Published online October 21, 2021.doi: 10.1136/neurintsurg-2021-017872

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  • 30

    Fu Q, Wang Y, Zhang Y, et al. Qualitative and quantitative wall enhancement on magnetic resonance imaging is associated with symptoms of unruptured intracranial aneurysms. Stroke. 2021;52(1):213222.

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  • 31

    Matsushige T, Shimonaga K, Ishii D, et al. Vessel wall imaging of evolving unruptured intracranial aneurysms. Stroke. 2019;50(7):18911894.

  • 32

    Larsen N, Flüh C, Saalfeld S, et al. Multimodal validation of focal enhancement in intracranial aneurysms as a surrogate marker for aneurysm instability. Neuroradiology. 2020;62(12):16271635.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Grüter BE, Wanderer S, Strange F, et al. Patterns of neointima formation after coil or stent treatment in a rat saccular sidewall aneurysm model. Stroke. 2021;52(3):10431052.

    • Crossref
    • PubMed
    • Search Google Scholar
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  • Collapse
  • Expand

Figure from Ramos et al. (pp 95–103).

  • FIG. 1.

    Representative cases of 3 AWE patterns evaluated with T1-weighted 3D black-blood fast spin echo MRI performed after contrast enhancement. A and B: CAWE and FAWE (arrows). C: No enhancement (arrowhead). The insets show the enhancement patterns.

  • FIG. 2.

    Distribution of AWE patterns in the unstable group. The CAWE pattern was significantly more frequent than the NAWE and FAWE patterns. *Significant at p < 0.05.

  • FIG. 3.

    An unruptured 8.7-mm right internal carotid artery–posterior communicating artery aneurysm. Native (A) and contrast-enhanced (B) VWI performed before endovascular treatment showed CAWE (white arrowheads). The aneurysm was completely obliterated with a VER of 21.9% by using the Neuroform stent (black arrowhead) (C). Follow-up imaging performed 6 months after treatment showed recurrence at the neck segment (black arrowhead) (D).

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    Nevzati E, Rey J, Coluccia D, et al. Aneurysm wall cellularity affects healing after coil embolization: assessment in a rat saccular aneurysm model. J Neurointerv Surg. 2020;12(6):621625.

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    Mascitelli JR, Moyle H, Oermann EK, et al. An update to the Raymond-Roy Occlusion Classification of intracranial aneurysms treated with coil embolization. J Neurointerv Surg. 2015;7(7):496502.

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    Greve T, Sukopp M, Wostrack M, Burian E, Zimmer C, Friedrich B. Initial Raymond-Roy Occlusion Classification but not packing density defines risk for recurrence after aneurysm coiling. Clin Neuroradiol. 2021;31(2):391399.

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    Hashimoto Y, Matsushige T, Kawano R, et al. Segmentation of aneurysm wall enhancement in evolving unruptured intracranial aneurysms. J Neurosurg. 2021;136(2):449455.

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    Feng MT, Wen WL, Feng ZZ, Fang YB, Liu JM, Huang QH. Endovascular embolization of intracranial aneurysms: to use stent(s) or not? Systematic review and meta-analysis. World Neurosurg. 2016;93:271278.

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  • 23

    Zhang X, Zuo Q, Tang H, et al. Stent assisted coiling versus non-stent assisted coiling for the management of ruptured intracranial aneurysms: a meta-analysis and systematic review. J Neurointerv Surg. 2019;11(5):489496.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Bavinzski G, Talazoglu V, Killer M, et al. Gross and microscopic histopathological findings in aneurysms of the human brain treated with Guglielmi detachable coils. J Neurosurg. 1999;91(2):284293.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Brinjikji W, Kallmes DF, Kadirvel R. Mechanisms of healing in coiled intracranial aneurysms: a review of the literature. AJNR Am J Neuroradiol. 2015;36(7):12161222.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Dai D, Ding YH, Danielson MA, et al. Histopathologic and immunohistochemical comparison of human, rabbit, and swine aneurysms embolized with platinum coils. AJNR Am J Neuroradiol. 2005;26(10):25602568.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Groden C, Hagel C, Delling G, Zeumer H. Histological findings in ruptured aneurysms treated with GDCs: six examples at varying times after treatment. AJNR Am J Neuroradiol. 2003;24(4):579584.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Szikora I, Seifert P, Hanzely Z, et al. Histopathologic evaluation of aneurysms treated with Guglielmi detachable coils or matrix detachable microcoils. AJNR Am J Neuroradiol. 2006;27(2):283288.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Wang C, Li M, Chen H, Yang X, Zhang Y, Zhang D. Histopathological analysis of in vivo specimens of recurrent aneurysms after coil embolization. J Neurointerv Surg. Published online October 21, 2021.doi: 10.1136/neurintsurg-2021-017872

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Fu Q, Wang Y, Zhang Y, et al. Qualitative and quantitative wall enhancement on magnetic resonance imaging is associated with symptoms of unruptured intracranial aneurysms. Stroke. 2021;52(1):213222.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Matsushige T, Shimonaga K, Ishii D, et al. Vessel wall imaging of evolving unruptured intracranial aneurysms. Stroke. 2019;50(7):18911894.

  • 32

    Larsen N, Flüh C, Saalfeld S, et al. Multimodal validation of focal enhancement in intracranial aneurysms as a surrogate marker for aneurysm instability. Neuroradiology. 2020;62(12):16271635.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Grüter BE, Wanderer S, Strange F, et al. Patterns of neointima formation after coil or stent treatment in a rat saccular sidewall aneurysm model. Stroke. 2021;52(3):10431052.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

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