High-resolution magnetic resonance vessel wall imaging–guided endovascular recanalization for nonacute intracranial artery occlusion

Zhikai Hou Department of Interventional Neuroradiology, Beijing Tiantan Hospital, Capital Medical University, Beijing, China;
China National Clinical Research Center for Neurological Diseases, Beijing, China;

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Long Yan Department of Interventional Neuroradiology, Beijing Tiantan Hospital, Capital Medical University, Beijing, China;
China National Clinical Research Center for Neurological Diseases, Beijing, China;

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Zhe Zhang China National Clinical Research Center for Neurological Diseases, Beijing, China;
Tiantan Neuroimaging Center of Excellence, Beijing Tiantan Hospital, Capital Medical University, Beijing, China;

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Jing Jing China National Clinical Research Center for Neurological Diseases, Beijing, China;
Tiantan Neuroimaging Center of Excellence, Beijing Tiantan Hospital, Capital Medical University, Beijing, China;
Department of Neurology, Beijing Tiantan Hospital, Capital Medical University, Beijing, China;

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Jinhao Lyu Department of Radiology, The First Medical Center of Chinese PLA General Hospital, Beijing, China; and

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Ferdinand K. Hui Radiology and Radiological Science, Johns Hopkins Hospital, Baltimore, Maryland

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Weilun Fu Department of Interventional Neuroradiology, Beijing Tiantan Hospital, Capital Medical University, Beijing, China;
China National Clinical Research Center for Neurological Diseases, Beijing, China;

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Ying Yu Department of Interventional Neuroradiology, Beijing Tiantan Hospital, Capital Medical University, Beijing, China;
China National Clinical Research Center for Neurological Diseases, Beijing, China;

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Rongrong Cui Department of Interventional Neuroradiology, Beijing Tiantan Hospital, Capital Medical University, Beijing, China;
China National Clinical Research Center for Neurological Diseases, Beijing, China;

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Min Wan Department of Interventional Neuroradiology, Beijing Tiantan Hospital, Capital Medical University, Beijing, China;
China National Clinical Research Center for Neurological Diseases, Beijing, China;

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Jia Song Department of Interventional Neuroradiology, Beijing Tiantan Hospital, Capital Medical University, Beijing, China;
China National Clinical Research Center for Neurological Diseases, Beijing, China;

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Yongjun Wang China National Clinical Research Center for Neurological Diseases, Beijing, China;
Tiantan Neuroimaging Center of Excellence, Beijing Tiantan Hospital, Capital Medical University, Beijing, China;
Department of Neurology, Beijing Tiantan Hospital, Capital Medical University, Beijing, China;

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Zhongrong Miao Department of Interventional Neuroradiology, Beijing Tiantan Hospital, Capital Medical University, Beijing, China;
China National Clinical Research Center for Neurological Diseases, Beijing, China;

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Xin Lou Department of Radiology, The First Medical Center of Chinese PLA General Hospital, Beijing, China; and

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Ning Ma Department of Interventional Neuroradiology, Beijing Tiantan Hospital, Capital Medical University, Beijing, China;
China National Clinical Research Center for Neurological Diseases, Beijing, China;

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OBJECTIVE

On the basis of the characteristics of occluded segments on high-resolution magnetic resonance vessel wall imaging (MR-VWI), the authors evaluated the role of high-resolution MR-VWI–guided endovascular recanalization for patients with symptomatic nonacute intracranial artery occlusion (ICAO).

METHODS

Consecutive patients with symptomatic nonacute ICAO that was refractory to aggressive medical treatment were prospectively enrolled and underwent endovascular recanalization. High-resolution MR-VWI was performed before the recanalization intervention. The characteristics of the occluded segments on MR-VWI, including signal intensity, occlusion morphology, occlusion angle, and occlusion length, were evaluated. Technical success was defined as arterial recanalization with modified Thrombolysis in Cerebral Infarction grade 2b or 3 and residual stenosis < 50%. Perioperative complications were recorded. The characteristics of the occluded segments on MR-VWI were compared between the recanalized group and the failure group.

RESULTS

Twenty-five patients with symptomatic nonacute ICAO that was refractory to aggressive medical treatment were consecutively enrolled from April 2020 to February 2021. Technical success was achieved in 19 patients (76.0%). One patient (4.0%) had a nondisabling ischemic stroke during the perioperative period. Multivariable logistic analysis showed that successful recanalization of nonacute ICAO was associated with occlusion with residual lumen (OR 0.057, 95% CI 0.004–0.735, p = 0.028) and shorter occlusion length (OR 0.853, 95% CI 0.737–0.989, p = 0.035).

CONCLUSIONS

The high-resolution MR-VWI modality could be used to guide endovascular recanalization for nonacute ICAO. Occlusion with residual lumen and shorter occlusion length on high-resolution MR-VWI were identified as predictors of technical success of endovascular recanalization for nonacute ICAO.

ABBREVIATIONS

ICAO = intracranial artery occlusion; IQR = interquartile range; MR-VWI = magnetic resonance vessel wall imaging; TICI = Thrombolysis in Cerebral Infarction.

OBJECTIVE

On the basis of the characteristics of occluded segments on high-resolution magnetic resonance vessel wall imaging (MR-VWI), the authors evaluated the role of high-resolution MR-VWI–guided endovascular recanalization for patients with symptomatic nonacute intracranial artery occlusion (ICAO).

METHODS

Consecutive patients with symptomatic nonacute ICAO that was refractory to aggressive medical treatment were prospectively enrolled and underwent endovascular recanalization. High-resolution MR-VWI was performed before the recanalization intervention. The characteristics of the occluded segments on MR-VWI, including signal intensity, occlusion morphology, occlusion angle, and occlusion length, were evaluated. Technical success was defined as arterial recanalization with modified Thrombolysis in Cerebral Infarction grade 2b or 3 and residual stenosis < 50%. Perioperative complications were recorded. The characteristics of the occluded segments on MR-VWI were compared between the recanalized group and the failure group.

RESULTS

Twenty-five patients with symptomatic nonacute ICAO that was refractory to aggressive medical treatment were consecutively enrolled from April 2020 to February 2021. Technical success was achieved in 19 patients (76.0%). One patient (4.0%) had a nondisabling ischemic stroke during the perioperative period. Multivariable logistic analysis showed that successful recanalization of nonacute ICAO was associated with occlusion with residual lumen (OR 0.057, 95% CI 0.004–0.735, p = 0.028) and shorter occlusion length (OR 0.853, 95% CI 0.737–0.989, p = 0.035).

CONCLUSIONS

The high-resolution MR-VWI modality could be used to guide endovascular recanalization for nonacute ICAO. Occlusion with residual lumen and shorter occlusion length on high-resolution MR-VWI were identified as predictors of technical success of endovascular recanalization for nonacute ICAO.

In Brief

Researchers evaluated the role of high-resolution magnetic resonance vessel wall imaging (MR-VWI) for endovascular recanalization of nonacute intracranial artery occlusion (ICAO). Successful recanalization of nonacute ICAO was associated with occlusion with residual lumen and shorter occlusion length on high-resolution MR-VWI. These results indicated that high-resolution MR-VWI can display the characteristics of occluded arterial segments and guide endovascular recanalization of nonacute ICAO.

Intracranial artery occlusion (ICAO) is one of the conditions of advanced intracranial artery atherosclerosis.1,2 Previous randomized trials have shown that mechanical thrombectomy is overwhelmingly superior to medical treatment for patients with acute intracranial large-vessel occlusion involving the anterior territory.3 However, patients with nonacute ICAO, especially those with hemodynamic compromise, have higher risks of recurrent stroke even with aggressive medical treatment.4,5 Recent studies have shown that endovascular recanalization of nonacute ICAO may be an effective treatment approach for these patients.6–9

Endovascular recanalization for nonacute ICAO has heterogeneous outcomes and perioperative complications. The technical success rate of recanalization for nonacute ICAO ranges from 53.1% to 92.3%.10–12 The perioperative complication rate is 14.3%–30.7%, which includes vessel perforation, dissection, thromboembolism, in-stent thrombosis, and hyperperfusion injury.10–12 Previous studies demonstrated that successful recanalization of chronic carotid occlusion was associated with occlusion length and morphology of the responsible arteries.13 It remains unclear whether the characteristics of intracranial occluded segments are associated with successful recanalization of nonacute ICAO. High-resolution magnetic resonance vessel wall imaging (MR-VWI) can be used to directly visualize and provide detailed information about intracranial occluded segments. In our study, we explored the characteristics of occluded segments on high-resolution MR-VWI and assessed the role of MR-VWI in endovascular recanalization for nonacute ICAO.

Methods

Study Population

This was a prospective, exploratory study of consecutive patients with symptomatic nonacute ICAO who were treated by the endovascular treatment team of a national stroke center from April 2020 to February 2021. ICAO was confirmed with magnetic resonance angiography, computed tomography angiography, or digital subtraction angiography. These patients did not achieve intravenous thrombolysis or undergo mechanical thrombectomy because of a minor stroke (defined as National Institutes of Health Stroke Scale score < 4) or an excessive long time interval for intravenous thrombolysis. Aggressive medical treatment, including dual antiplatelet therapy, intensive lipid-lowering therapy, and risk factor management, were prescribed. All patients had ICAO that was refractory to aggressive medical treatment and had recurrent ischemic stroke or transient ischemic attack. Recurrent ischemic stroke was defined as a new sudden-onset focal neurological deficit due to ischemic stroke in the territory of the occluded artery that was confirmed with diffusion-weighted imaging. Recurrent transient ischemic attack was defined as the clinical syndrome of acute focal loss of brain function related to the occluded artery, with symptoms resolved within 24 hours.

The inclusion criteria were the following: 1) age ≥ 18 years; 2) recurrent ischemic stroke or transient ischemic attack in the territory of the responsible arteries that received aggressive medical treatment; 3) duration from last qualifying event to endovascular treatment greater than 24 hours; 4) total ICAO of the intracranial internal carotid artery, middle cerebral artery, basilar artery, and intracranial vertebral artery verified with digital subtraction angiography (modified Thrombolysis in Cerebral Infarction [TICI] grade 0); and 5) two or more atherosclerotic risk factors such as hypertension, hyperlipidemia, diabetes mellitus, and cigarette smoking.

Patients who met the following exclusion criteria were not considered for recanalization: 1) nonatherosclerotic diseases such as suspected cerebral vasculitis, arterial dissection, and moyamoya disease; and 2) concomitant cerebral arteriovenous malformation, dural arteriovenous fistula, and intracranial aneurysm proximal or distal to the occlusive artery.

The study protocol was approved by the institutional review board of Beijing Tiantan Hospital. Written informed consent was obtained from the patients or their legal guardians. The data for the analyses described in this article are available on request to the corresponding author.

MR-VWI Protocols

All patients underwent high-resolution MR-VWI before the recanalization procedure. High-resolution T1-weighted MR-VWI was performed with a 3-T MR scanner (MAGNETOM Prisma, Siemens Healthineers) and 64-channel head/neck coil. MR-VWI was performed using 3D T1-weighted turbo spin-echo sequences with the following parameters: repetition time/echo time 760/15 msec; slice partial Fourier factor 0.75; turbo factor 60; echo spacing 4.52 msec; parallel imaging acceleration 3; field of view 240 mm × 220 mm × 172 mm (foot-head × anterior-posterior × right-left); and voxel size 0.54 mm × 0.54 mm × 0.54 mm. The scan time for MR-VWI was 6 minutes 57 seconds. Other MRI scans included those obtained with diffusion-weighted imaging, noncontrast MR angiography, susceptibility-weighted imaging, and T2-weighted imaging.

Evaluation of Vessel Wall Characteristics

All images of the responsible lesions obtained with high-resolution MR-VWI were reconstructed and processed using commercially available software (VesselMass, Leiden University Medical Center). All evaluations were performed on reformatted images. Vessel wall signal intensity was classified as hypointense, isointense, and hyperintense compared with adjacent cortical gray matter. Occlusion morphologies were reanalyzed on MR-VWI and characterized as either total occlusion or occlusion with residual lumen. Total occlusions were segments that were devoid of flow on digital subtraction angiography and showed vessel collapse or total luminal filling defects on MR-VWI. Occlusions with residual lumen were defined as segments that were invisible on digital subtraction angiography but had visible residual flow voids on MR-VWI within the segment. Total occlusion length was automatically calculated by the software after we manually traced the longitudinal axis of the vasculature. The occlusion angle was defined as the degree of angulation of the occluded segment, with a straight occluded segment defined as 180°.

All vessel wall images were interpreted in consensus by two neurologists (Z.H. with 3 years of experience and J.J. with 5 years) who were blinded to the clinical and procedural information. A third reader (X.L. with more than 10 years of experience) was invited to resolve disagreements when they occurred. To evaluate interobserver agreement regarding occlusion morphology, three investigators (Z.H., J.J., and X.L.) independently classified occlusion morphology in all cases.

Endovascular Recanalization Procedures

All patients underwent the endovascular recanalization procedure after receiving the dual antiplatelet regimen of aspirin (100 mg/day) and clopidogrel (75 mg/day) for at least 5 days.

All procedures were performed under general anesthesia by a qualified neurointerventionalist (N.M.). After vascular access was achieved, intravenous heparin was administered via a bolus (75 U/kg), followed by half the dose 1 hour later; if the procedure lasted longer than 2 hours, a quarter of the initial dose was given every hour thereafter. The guide catheter was progressed into the cervical vertebral or internal carotid artery as high as allowed by vessel tortuosity. Under roadmap guidance, a microwire was advanced coaxially through a microcatheter to traverse the occluded segment. Then, the microwire was withdrawn, and microcatheter injection was performed to verify that the tip of the microcatheter was located in the true distal lumen. The microcatheter was then exchanged for the balloon catheter. Underdilation was used to avoid arterial dissection, vessel rupture, and the snowplow effect due to the compression of plaque into the perforator arteries. The balloon size was 80% of the actual luminal diameter, or 60% was used to treat lesions directly adjacent to angiographically visible perforators.14 A 9-mm-long or 15-mm-long balloon was preferred. If the occlusion length was more than 15 mm, multiple dilations from distal to proximal were used. After balloon dilation, angiography was conducted to evaluate the degree of residual stenosis and antegrade flow, which determined whether self-expanding stent implantation or balloon-mounted stent implantation was used as the endovascular treatment. If stent implantation was required, the stent size was determined on the basis of the proximal and distal diameters of the lesion, as well as the length of the occluded segment. Postprocedural angiography was performed to confirm patency and assess residual stenosis and antegrade flow. Technical success was defined as vessel recanalization with modified TICI grade 2b or 3 and residual stenosis < 50%.6

Noncontrast computed tomography was performed. Perioperative medical treatment was the same as described in a previous study.14 If blood pressure was greater than 140/90 mm Hg, oral or intravenous antihypertensive treatment was required to decrease the risk of hyperperfusion injury. Dual antiplatelet therapy was maintained for at least 3 months after the procedure.

Risk factors were controlled to achieve the following: systolic blood pressure less than 140 mm Hg (or 130 mm Hg in patients with diabetes mellitus); low-density lipoprotein less than 70 mg/dl or a decrease by 50%; smoking cessation; and lifestyle modifications.15

Statistical Analysis

Continuous variables are presented as mean ± SD or median (interquartile range [IQR]), and categorical variables are presented as percentages. Interobserver agreement regarding the occlusion morphologies was assessed using Fleiss’ kappa statistic. κ values > 0.80, 0.60–0.80, 0.40–0.60, and < 0.40 were considered to represent excellent, substantial, moderate, and poor agreement, respectively. Differences in categorical variables between the recanalized group and the failure group were assessed with the Fisher’s exact test. Differences in continuous variables between the two groups were assessed using the Student t-test or Mann-Whitney U-test. The association between vessel wall characteristics on high-resolution MR-VWI and technical success was further assessed with multivariable logistics analysis (adjusted for age and sex). A 2-sided p value < 0.05 indicated statistical significance. All statistical analyses were performed using commercial SPSS software version 26.0 (IBM Corp.).

Results

Patient Baseline Features

Twenty-five patients with nonacute ICAO that was refractory to aggressive medical treatment were consecutively enrolled from April 2020 to February 2021. Twenty-one (84.0%) patients had recurrent ischemic stroke, and 4 (16.0%) had recurrent transient ischemic attacks. The mean ± SD age was 53.4 ± 10.6 years. There are 18 (72.0%) men and 7 (28.0%) women. The details of the vascular risk factors of the patients are summarized in Table 1. The median (IQR) time interval from occlusion imaging to high-resolution MR-VWI was 39.0 (29.0–61.0) days. The responsible arteries were the intracranial internal carotid arteries in 9 (36.0%) patients, the middle cerebral arteries in 8 (32.0%), the basilar arteries in 7 (28.0%), and the intracranial vertebral artery in 1 (4.0%). Technical success was achieved in 19 patients (76.0%). Among these patients, 10 underwent only balloon angioplasty. Balloon-mounted stents were used in 2 patients and self-expanding stents in 7. Six patients had procedural failure because the guidewire was unable to traverse the occluded segments. One (4.5%) patient with basilar artery occlusion had a thromboembolic event after the endovascular procedure. There were no instances of dissection or vessel perforation during the procedures.

TABLE 1.

Baseline clinical variables and vessel wall characteristics

VariableTotal (n = 25)Recanalized Group (n = 19)Failure Group (n = 6)p Value
Male sex18 (72.0)14 (73.7)4 (66.7)>0.99
Age, yrs53.4 ± 10.653.0 ± 10.254.8 ± 12.40.719
Hypertension16 (64.0)11 (57.9)5 (83.3)0.364
Diabetes10 (40.0)6 (31.6)4 (66.7)0.175
Hyperlipidemia10 (40.0)9 (47.4)1 (16.7)0.345
Smoking15 (60.0)12 (63.2)3 (50.0)0.653
Responsible artery0.129
 Anterior circulation17 (68.0)11 (57.9)6 (100.0)
 Posterior circulation8 (32.0)8 (42.1)0 (0.0)
Occlusion imaging to MR-VWI, days39.0 (29.0–61.0)40.0 (29.0–58.0)36.0 (27.5–145.3)0.726
MR-VWI to recanalization, days3.0 (2.0–4.0)3.0 (2.0–4.0)3.5 (2.8–4.3)0.695
MR-VWI characteristics
 Signal intensity>0.99
  Hyperintense4 (16.0)3 (15.8)1 (16.7)
  Isointense21 (84.0)16 (84.2)5 (83.3)
 Occlusion morphology0.032
  Occlusion w/ residual lumen18 (72.0)16 (84.2)2 (33.3)
  Total occlusion7 (28.0)3 (15.8)4 (66.7)
 Occlusion angle, °145.6 (122.9–180.0)153.3 (128.3–180.0)119.1 (106.0–148.8)0.028
 Occlusion length, mm21.2 ± 8.419.0 ± 6.928.3 ± 9.40.015

Values are shown as number (%), mean ± SD, or median (IQR) unless indicated otherwise.

Characteristics of the Occluded Segments on High-Resolution MR-VWI

The signal intensities of occluded segments on high-resolution MR-VWI were isointense in 21 (84.0%) patients and hyperintense in 4 (16.0%). There were 18 (72.0%) patients with occlusions with residual lumen and 7 (28.0%) with total occlusions on MR-VWI. Interobserver agreement regarding occlusion morphology was excellent (Fleiss’ κ = 0.848). The median (IQR) occlusion angle on MR-VWI was 145.6° (122.9°–180.0°). The mean ± SD occlusion length on MR-VWI was 21.2 ± 8.4 mm (Table 1).

Comparison of Baseline Features and Occluded Segment Characteristics Between the Recanalized Group and Failure Group

There were no significant differences in terms of age, sex, vascular risk factors, or distributions of the responsible arteries. The time intervals from imaging occlusion to MR-VWI were similar between the two groups. The signal intensities of the occluded segments showed no statistical differences between the two groups. Compared with the failure group, the recanalized group had more patients with occlusions with residual lumen (84.2% vs 33.3%) and fewer patients with total occlusions (15.8% vs 66.7%, p = 0.032). The recanalized group had a larger median occlusion angle (153.3° vs 119.1°, p = 0.028) and a shorter mean occlusion length (19.0 mm vs 28.3 mm, p = 0.015) than the failure group (Figs. 1 and 2).

FIG. 1.
FIG. 1.

A patient with symptomatic middle cerebral artery occlusion underwent endovascular recanalization, which was unsuccessful because the guidewire could not be advanced through the occlusion. A: Digital subtraction angiography demonstrated total occlusion of the left middle cerebral artery. B: Longitudinal vessel wall imaging showed that the vessel lumen was completely occluded with a fully collapsed vessel wall (arrowheads), and the occlusion length was 37.51 mm (arrows). C: The occluded segment made a 107.8° turn from the proximal to the distal M1 segment. Figure is available in color online only.

FIG. 2.
FIG. 2.

A patient with symptomatic basilar artery occlusion was predilated with a 2 × 15–mm Gateway catheter and then stented with the 3 × 15–mm Wingspan stent system (Boston Scientific). A: Preprocedural digital subtraction angiography demonstrated total occlusion of the basilar artery. B: Longitudinal vessel wall imaging showed a visible residual lumen within the occluded segment (arrowheads), and the occlusion length was 20.50 mm (arrows). C: The occluded segment had a 136.3° turn. D: Postprocedural digital subtraction angiography demonstrated technically successful recanalization with TICI grade 3. Figure is available in color online only.

Multivariable logistic analysis showed that occlusion with residual lumen (OR 0.057, 95% CI, 0.004–0.735, p = 0.028) and occlusion length (OR 0.853, 95% CI 0.737–0.989, p = 0.035) were associated with technical success of endovascular recanalization for nonacute ICAO (Table 2).

TABLE 2.

Multivariable analysis of vessel wall characteristics on MR-VWI between the two groups

VariableAdjusted OR (95% CI)p Value
Occlusion w/ residual lumen0.057 (0.004–0.735)0.028
Occlusion angle, °1.037 (0.994–1.081)0.093
Occlusion length, mm0.853 (0.737–0.989)0.035

Discussion

In this prospective study, we found that high-resolution MR-VWI can provide further insight into the occluded segment of nonacute ICAO, including vessel wall signal intensity, occlusion morphology, occlusion angle, and occlusion length. Successful recanalization was associated with occlusion with residual lumen and shorter occlusion length on high-resolution MR-VWI. The associations of technical success of endovascular recanalization for nonacute ICAO with vessel wall characteristics on high-resolution MR-VWI are not well established in the literature.

In our study, 19 (76.0%) patients achieved technical success of endovascular recanalization. This technical success rate is comparable to those of a recently reported case series. Previous studies reported technical success rates of 53.1%–92.3% for endovascular recanalization of nonacute ICAO.10–12 The differences in the endovascular recanalization rates of these studies may be due to varying intracranial occlusion locations, characteristics of occluded segments, and time intervals from vessel occlusion to endovascular recanalization.

One (4.0%) patient had ischemic stroke caused by embolism during the perioperative period. Retrospective studies have reported perioperative complication rates from 14.3% to 30.7%,10,11,16,17 which are higher than the rate of our study. The potential reason may be because high-resolution MR-VWI provided information about the occluded segments, such as occlusion morphology, angle, and length. Microwire navigation without guidance risks damage to the vessel wall of the occluded segments. The occlusion angle and length on high-resolution MR-VWI allow the operator to have a better and direct understanding of the lesion. Endovascular recanalization may be safer with the guidance of high-resolution MR-VWI.

The study showed that occlusion with residual lumen was associated with successful recanalization. The recanalized group had more patients with occlusions with residual lumen than the failure group (84.2% vs 33.3%, p = 0.032). We classified the occlusive morphologies as total occlusion or occlusion with residual lumen on the basis of findings on MR-VWI. Luminal filling of the vessel disappeared and the vessel wall fully collapsed in the patients included in the total occlusions group. A possible reason was that the occlusion time was too long and the structure changed in the occluded segments. Consequently, it was difficult to traverse the occluded lesions with the microwire in order to reach the distal lumen. This may explain why recanalization was difficult in patients with total occlusions. The vessel wall signal intensities of the two groups were statistically similar, which needs to be further validated with a larger sample size.

This study found that the median occlusion length was shorter in the recanalized group than the failure group (19.0 mm vs 28.3 mm, p = 0.015). Similar findings were found in previous studies of endovascular recanalization for chronic coronary occlusion or chronic internal carotid artery occlusion. Occlusion length > 20 mm has been confirmed as an independent predictor of successful recanalization for chronic coronary occlusion.14 Among patients with chronic internal carotid artery occlusion, occlusion length was also shorter in the procedural success group than the unsuccessful group (54 mm vs 75 mm, p < 0.001).15 In theory, microwire navigation through the longer ICAO is more difficult and easily induces arterial dissection. Therefore, longer ICAO occlusion would reduce the technical success rate.

In the previous study, the occlusion length of the intracranial artery was a straight-line distance rather than the actual distance between the proximal and distal sites of the occluded segments on the angiogram.6,8,13 In our study, we calculated the actual occlusion length on reformatted vessel wall images. High-resolution MR-VWI can display the proximal and distal sites of the occluded segments. It is quite difficult to identify the distal site of an ICAO on angiography, especially those in the intracranial internal carotid artery and vertebral artery. A previous study of chronic ICAO visualized the distal sites of the occluded segments with the dual-roadmap technique, which had the disadvantages of increased procedural complexity and overuse of contrast medium.7

In this study, the occlusion angle was larger in the recanalized group than the failure group (153.3° vs 119.1°, p = 0.028). However, the association of occlusion angle with technical success of recanalization had no statistical difference after adjustment for confounding factors. In our study, the occlusion angle was calculated as the intersection angle between the proximal and distal segments of the occlusion lesion. In practice, the microwire may traverse the occluded segment smoothly when a larger occlusion angle is present. A study with a larger sample size is needed to confirm this finding in the future.

In addition, previous studies have shown the association between the technical success of recanalization for nonacute ICAO and the time interval between vessel occlusion and endovascular recanalization.10,18 However, in this study, the time interval between occlusion imaging and recanalization was not statistically different between the two groups. This finding may be partially explained by the short time interval (median 39.0 days) from occlusion imaging to MR-VWI for the enrolled patients in this study.

There were several limitations in our study. First, this was a single-center study with a limited sample size of patients restricted to the Chinese population, which may have caused type II error. Second, the characteristics of the occluded segments on high-resolution MR-VWI may have changed over the time interval from vessel occlusion to recanalization. Studies with larger sample sizes are needed to explore the associations of the characteristics of occluded segments with the technical success of recanalization in patients with different stages of ICAO. Third, the technical difficulty of endovascular recanalization may vary among different sites of ICAO. We did not compare different intracranial arteries because of the small sample size. The study findings need to be confirmed in a larger cohort study in the future.

Conclusions

The high-resolution MR-VWI modality may be a promising and useful tool in the clinical practice for endovascular recanalization of nonacute ICAO. The characteristics of the occluded segments, such as signal intensity, occlusion morphology, occlusion angle, and occlusion length, can be revealed using high-resolution MR-VWI. Successful recanalization of nonacute ICAO may be associated with occlusion with residual lumen and shorter occlusion length on high-resolution MR-VWI. These findings need to be confirmed with further prospective and multicenter studies.

Acknowledgments

We thank Dr. Mengxing Wang from China National Clinical Research Center for Neurological Disease, Beijing, China, for her assistance with statistical analysis. We thank Dr. Shimeng Liu from the Department of Neurology, Beijing Tiantan Hospital, Capital Medical University, Beijing, China, for her assistance with text editing. This work was supported by the Beijing Yangfan Plan (contract grant no. XMLX201844 awarded to N.M.) and National Natural Science Foundation of China (contract grant nos. 81825012 and 81730048 awarded to X.L.).

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: Ma, Hou, Yan, Zhang, Jing, Lou. Acquisition of data: Ma, Hou, Yan, Jing, Fu, Yu, Cui, Wan, Song. Analysis and interpretation of data: Ma, Hou, Yan, Zhang, Jing, Lou. Drafting the article: Ma, Hou, Yan. Critically revising the article: Ma, Hou, Yan, Jing, Lyu, Hui, Lou. Reviewed submitted version of manuscript: Ma, Hou, Yan, Zhang, Jing, Lyu, Hui, Fu, Yu, Cui, Wan, Song, Miao, Lou. Approved the final version of the manuscript on behalf of all authors: Ma. Statistical analysis: Ma, Hou. Administrative/technical/material support: Ma. Study supervision: Ma, Wang, Miao, Lou.

Supplemental Information

Online-Only Content

Supplemental material is available with the online version of the article.

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  • 5

    Kuroda S, Houkin K, Kamiyama H, Mitsumori K, Iwasaki Y, Abe H. Long-term prognosis of medically treated patients with internal carotid or middle cerebral artery occlusion: can acetazolamide test predict it? Stroke. 2001;32(9):21102116.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Gao F, Guo X, Han J, Sun X, Zhuo Z, Miao Z. Endovascular recanalization for symptomatic non-acute middle cerebral artery occlusion: proposal of a new angiographic classification. J Neurointerv Surg. 2021;13(10):900905.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Gao F, Guo X, Sun X, Liu Y, Wu Y, Miao Z. Dual-roadmap guidance for endovascular recanalization of medically refractory non-acute intracranial arterial occlusions: consecutive multicenter series and technical review. J Neurointerv Surg. 2021;13(10):889893.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Gao F, Sun X, Guo X, Li D, Xu GD, Miao ZR. Endovascular recanalization of symptomatic nonacute intracranial internal carotid artery occlusion: proposal of a new angiographic classification. AJNR Am J Neuroradiol. 2021;42(2):299305.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Gao F, Sun X, Zhang H, Ma N, Mo D, Miao Z. Endovascular recanalization for nonacute intracranial vertebral artery occlusion according to a new classification. Stroke. 2020;51(11):33403343.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Yao YD, Liu AF, Qiu HC, Zhou J, Li C, Wang Q, et al. Outcomes of late endovascular recanalization for symptomatic non-acute atherosclerotic intracranial large artery occlusion. Clin Neurol Neurosurg. 2019;187:105567.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Ma L, Liu YH, Feng H, Xu JC, Yan S, Han HJ, et al. Endovascular recanalization for symptomatic subacute and chronic intracranial large artery occlusion of the anterior circulation: initial experience and technical considerations. Neuroradiology. 2019;61(7):833842.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    PH, Park JW, Park S, Kim JL, Lee DH, Kwon SU, et al. Intracranial stenting of subacute symptomatic atherosclerotic occlusion versus stenosis. Stroke. 2011;42(12):34703476.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Chen YH, Leong WS, Lin MS, Huang CC, Hung CS, Li HY, et al. Predictors for successful endovascular intervention in chronic carotid artery total occlusion. JACC Cardiovasc Interv. 2016;9(17):18251832.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Alexander MJ, Zauner A, Chaloupka JC, Baxter B, Callison RC, Gupta R, et al. WEAVE trial: final results in 152 on-label patients. Stroke. 2019;50(4):889894.

  • 15

    Chimowitz MI, Lynn MJ, Derdeyn CP, Turan TN, Fiorella D, Lane BF, et al. Stenting versus aggressive medical therapy for intracranial arterial stenosis. N Engl J Med. 2011;365(11):9931003.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Gao P, Wang Y, Ma Y, Yang Q, Song H, Chen Y, et al. Endovascular recanalization for chronic symptomatic intracranial vertebral artery total occlusion: experience of a single center and review of literature. J Neuroradiol. 2018;45(5):295304.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    He Y, Bai W, Li T, Xue J, Wang Z, Zhu L, Hui F. Perioperative complications of recanalization and stenting for symptomatic nonacute vertebrobasilar artery occlusion. Ann Vasc Surg. 2014;28(2):386393.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Yang Y, Liu X, Wang R, Zhang Y, Zhang D, Zhao J. A treatment option for symptomatic chronic complete internal carotid artery occlusion: hybrid surgery. Front Neurosci. 2020;14 392.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

Supplementary Materials

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  • Expand

Images from Minchev et al. (pp 479–488).

  • FIG. 1.

    A patient with symptomatic middle cerebral artery occlusion underwent endovascular recanalization, which was unsuccessful because the guidewire could not be advanced through the occlusion. A: Digital subtraction angiography demonstrated total occlusion of the left middle cerebral artery. B: Longitudinal vessel wall imaging showed that the vessel lumen was completely occluded with a fully collapsed vessel wall (arrowheads), and the occlusion length was 37.51 mm (arrows). C: The occluded segment made a 107.8° turn from the proximal to the distal M1 segment. Figure is available in color online only.

  • FIG. 2.

    A patient with symptomatic basilar artery occlusion was predilated with a 2 × 15–mm Gateway catheter and then stented with the 3 × 15–mm Wingspan stent system (Boston Scientific). A: Preprocedural digital subtraction angiography demonstrated total occlusion of the basilar artery. B: Longitudinal vessel wall imaging showed a visible residual lumen within the occluded segment (arrowheads), and the occlusion length was 20.50 mm (arrows). C: The occluded segment had a 136.3° turn. D: Postprocedural digital subtraction angiography demonstrated technically successful recanalization with TICI grade 3. Figure is available in color online only.

  • 1

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    Wong LK. Global burden of intracranial atherosclerosis. Int J Stroke. 2006;1(3):158159.

  • 3

    Goyal M, Menon BK, van Zwam WH, Dippel DW, Mitchell PJ, Demchuk AM, et al. Endovascular thrombectomy after large-vessel ischaemic stroke: a meta-analysis of individual patient data from five randomised trials. Lancet. 2016;387(10029):17231731.

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    Yamauchi H, Higashi T, Kagawa S, Kishibe Y, Takahashi M. Chronic hemodynamic compromise and cerebral ischemic events in asymptomatic or remote symptomatic large-artery intracranial occlusive disease. AJNR Am J Neuroradiol. 2013;34(9):17041710.

    • Crossref
    • PubMed
    • Search Google Scholar
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  • 5

    Kuroda S, Houkin K, Kamiyama H, Mitsumori K, Iwasaki Y, Abe H. Long-term prognosis of medically treated patients with internal carotid or middle cerebral artery occlusion: can acetazolamide test predict it? Stroke. 2001;32(9):21102116.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Gao F, Guo X, Han J, Sun X, Zhuo Z, Miao Z. Endovascular recanalization for symptomatic non-acute middle cerebral artery occlusion: proposal of a new angiographic classification. J Neurointerv Surg. 2021;13(10):900905.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Gao F, Guo X, Sun X, Liu Y, Wu Y, Miao Z. Dual-roadmap guidance for endovascular recanalization of medically refractory non-acute intracranial arterial occlusions: consecutive multicenter series and technical review. J Neurointerv Surg. 2021;13(10):889893.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Gao F, Sun X, Guo X, Li D, Xu GD, Miao ZR. Endovascular recanalization of symptomatic nonacute intracranial internal carotid artery occlusion: proposal of a new angiographic classification. AJNR Am J Neuroradiol. 2021;42(2):299305.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Gao F, Sun X, Zhang H, Ma N, Mo D, Miao Z. Endovascular recanalization for nonacute intracranial vertebral artery occlusion according to a new classification. Stroke. 2020;51(11):33403343.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Yao YD, Liu AF, Qiu HC, Zhou J, Li C, Wang Q, et al. Outcomes of late endovascular recanalization for symptomatic non-acute atherosclerotic intracranial large artery occlusion. Clin Neurol Neurosurg. 2019;187:105567.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Ma L, Liu YH, Feng H, Xu JC, Yan S, Han HJ, et al. Endovascular recanalization for symptomatic subacute and chronic intracranial large artery occlusion of the anterior circulation: initial experience and technical considerations. Neuroradiology. 2019;61(7):833842.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    PH, Park JW, Park S, Kim JL, Lee DH, Kwon SU, et al. Intracranial stenting of subacute symptomatic atherosclerotic occlusion versus stenosis. Stroke. 2011;42(12):34703476.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Chen YH, Leong WS, Lin MS, Huang CC, Hung CS, Li HY, et al. Predictors for successful endovascular intervention in chronic carotid artery total occlusion. JACC Cardiovasc Interv. 2016;9(17):18251832.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Alexander MJ, Zauner A, Chaloupka JC, Baxter B, Callison RC, Gupta R, et al. WEAVE trial: final results in 152 on-label patients. Stroke. 2019;50(4):889894.

  • 15

    Chimowitz MI, Lynn MJ, Derdeyn CP, Turan TN, Fiorella D, Lane BF, et al. Stenting versus aggressive medical therapy for intracranial arterial stenosis. N Engl J Med. 2011;365(11):9931003.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Gao P, Wang Y, Ma Y, Yang Q, Song H, Chen Y, et al. Endovascular recanalization for chronic symptomatic intracranial vertebral artery total occlusion: experience of a single center and review of literature. J Neuroradiol. 2018;45(5):295304.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    He Y, Bai W, Li T, Xue J, Wang Z, Zhu L, Hui F. Perioperative complications of recanalization and stenting for symptomatic nonacute vertebrobasilar artery occlusion. Ann Vasc Surg. 2014;28(2):386393.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Yang Y, Liu X, Wang R, Zhang Y, Zhang D, Zhao J. A treatment option for symptomatic chronic complete internal carotid artery occlusion: hybrid surgery. Front Neurosci. 2020;14 392.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

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