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Clinical Relevance of Plaque Distribution for Basilar Artery Stenosis

Clinical Relevance of Plaque Distribution for Basilar Artery Stenosis Clinical Relevance of Plaque Distribution for Basilar Artery Stenosis J. Luo, X. Bai, K. Huang, T. Wang, R. Yang, L. Li, Q. Tian, R. Xu, T. Li, Y. Wang, Y. Chen, P. Gao, J. Chen, B. Yang, Y. Ma and L. Jiao AJNR Am J Neuroradiol 2023, 44 (5) 530-535 This information is current as doi: https://doi.org/10.3174/ajnr.A7839 of June 3, 2023. http://www.ajnr.org/content/44/5/530 ORIGINAL RESEARCH ADULT BRAIN Clinical Relevance of Plaque Distribution for Basilar Artery Stenosis J. Luo, X. Bai, K. Huang, T. Wang, R. Yang, L. Li, Q. Tian, R. Xu, T. Li, Y. Wang, Y. Chen, P. Gao, J. Chen, B. Yang, Y. Ma, and L. Jiao ABSTRACT BACKGROUND AND PURPOSE: There is no clear association between plaque distribution and postoperative complications in patients with basilar artery atherosclerotic stenosis. The aim of this study was to determine whether plaque distribution and post- operative complications after endovascular treatment for basilar artery stenosis are related. MATERIALS AND METHODS: Our study enrolled patients with severe basilar artery stenosis who were scanned with high-resolution MR imaging and followed by DSA before the intervention. According to high-resolution MR imaging, plaques can be classified as ven- tral, lateral, dorsal, or involved in 2 quadrants. Plaques affecting the proximal, distal, or junctional segments of the basilar artery were classified according to DSA. An experienced independent team assessed ischemic events after the intervention using MR imaging. Further analysis was conducted to determine the relationship between plaque distribution and postoperative complications. RESULTS: A total of 140 eligible patients were included in the study, with a postoperative complication rate of 11.4%. These patients were an average age of 61.9 (SD, 7.7) years. Dorsal wall plaques accounted for 34.3% of all plaques, and plaques distal to the ante- rior-inferior cerebellar artery accounted for 60.7%. Postoperative complications of endovascular treatment were associated with plaques located at the lateral wall (OR ¼ 4.00; 95% CI, 1.21–13.23; P ¼ .023), junctional segment (OR ¼ 8.75; 95% CI, 1.16–66.22; P ¼ .036), and plaque burden (OR ¼ 1.03; 95% CI, 1.01–1.06; P ¼ .042). CONCLUSIONS: Plaques with a large burden located at the junctional segment and lateral wall of the basilar artery may increase the likelihood of postoperative complications following endovascular therapy. A larger sample size is needed for future studies. ABBREVIATIONS: HR-MR imaging ¼ high-resolution MR imaging; LA ¼ lumen area; MLN ¼ maximal lumen narrowing; VA ¼ vessel area; WA ¼ wall area he basilar artery is the main artery for the posterior intracra- Patients with symptomatic and severe basilar artery stenosis Tnial circulation, where atherosclerotic stenosis is frequently ($70%) may benefit from endovascular treatment, including discovered in patients with ischemic events, such as stroke and primary angiography, balloon-mounted stent placement, and 1 2 TIA, which are responsible for 10.7% of strokes annually. self-expanding stent placement. Compared with the those in the anterior circulation, postoperative complications are higher in the posterior circulation with a reported risk of 21.6% in the Received November 20, 2022; accepted after revision March 1, 2023. 3,4 basilar artery. Therefore, it is crucial to understand and pre- From the China International Neuroscience Institute (J.L., X.B., T.W., R.Y., L.L., R.X., T.L., Y.W., Y.C., P.G., J.C., B.Y., Y.M., L.J.), Beijing, China; Department of Neurosurgery vent a high risk of complications occurring during endovascular (J.L., X.B., T.W., R.Y., L.L., R.X., T.L., Y.W., Y.C., P.G., J.C., B.Y., Y.M., L.J.), Xuanwu treatment in patients with basilar artery stenosis. Hospital, Beijing Key Laboratory of Clinical Epidemiology (Q.T.), School of Public Health, and Department of Interventional Radiology (P.G., L.J.), Xuanwu Hospital, The distribution of atherosclerotic plaques is associated with Capital Medical University, Beijing, China; and The Eighth Affiliated Hospital (K.H.), 5-7 the risk of ischemic events. For example, it is more likely that SUN YAT-SEN University, Shenzhen, Guangdong Province, China. atherosclerotic plaques located near perforating orifices are symp- This study was funded by the National Key Research and Development Program of China (2016YFC1301703), Beijing Science and Technology Planning Project tomatic during stent placement and may have a “snow plowing” (Z201100005520019), and Beijing Hospitals Authority's Ascent Plan (DFL20220702). effect. Several postmortem studies have demonstrated that basilar Please address correspondence to Liqun Jiao, MD, PhD, Departments of artery perforators typically originate from the lateral and dorsal Neurosurgery and Interventional Radiology, Xuanwu Hospital, Capital Medical University, No. 45 Changchun St, Xicheng District, 100053, Beijing, China; walls of the segment, distal from the anterior-inferior cerebellar e-mail: liqunjiao@sina.cn artery, possibly explaining the high rate of postoperative compli- Indicates open access to non-subscribers at www.ajnr.org 9,10 cations. However, the relationship between the distribution of basilar artery plaque and postoperative complications has not yet Indicates article with online supplemental data. http://dx.doi.org/10.3174/ajnr.A7839 been reported . 530 Luo May 2023 www.ajnr.org weakness; 3) treatment using endovascular therapy; 4) HR-MR imaging performed before the intervention; and 5) MR imaging performed before and within 72 hours after the intervention. The exclusion criteria were as follows: 1) stroke caused by occlu- sion of the basilar artery, 2) concurrent endovascular treatment of another intracranial or extracranial vessel, 3) basilar artery ste- nosis accompanied by moderate-to-severe vertebral artery stenosis, and 4) nonatherosclerotic causes (eg, Moyamoya disease, vasculitis, or dissection). Imaging Protocols and Evaluation FIG 1. A, The basilar artery is divided into 4 quadrants at the axial Before the intervention, all eligible patients were examined position based on high-resolution MR imaging. B, The basilar artery is using a 3T MR imaging scanner (Magnetom Spectra; Siemens) divided into 2 segments referring to the AICA on the basis of DSA, equipped with a standard 8-channel head coil. The scans were the proximal and distal segments. The junctional segment is defined when the plaque involves both segments across the anterior-inferior obtained using multiple sequences, including fast spin-echo T1- cerebellar artery. weighted imaging, TOF-MR angiography, and T1-weighted enhanced imaging. The parameters of the sequences are Understanding the distribution of basilar artery plaques can described in the Online Supplemental Data. HR-MR imaging help in reducing the incidence of postoperative complications. was acquired in the sagittal plane covering the basilar artery ves- Evidence from studies since the Stenting versus Aggressive Medical sel. Reconstruction of the axial, coronal, and sagittal views was Management for Preventing Recurrent Stroke in Intracranial required to analyze all the images. DSA examinations were also Stenosis (SAMMPRIS) trial has shown that the postoperative risk of performed for all the eligible patients. endovascular treatment for intracranial stenosis can be reduced An image core lab (http://imagecorelabcn.com/)was used to from 14.7% to 9.4% by excluding symptomatic patients with perfo- review all the images. The clinical data of patients were undisclosed rating infarction. The postoperative risk could be reduced exclud- and not included in the statistical analyses. Before the formal ing perforating infarction actually infers the plaque location, assessment, 5% of data from the analyzed cohort was used to train whether it is near perforating orifices, according to the phenotype of raters. Whenever the agreement was excellent (reliability, .0.75) cerebral infarction. Presently, plaque distribution in axial and coro- between 2 raters, the imaging data were formally evaluated. The nal positions can be precisely evaluated using high-resolution MR maximal lumen narrowing (MLN) or reference site, lumen diame- 12,13 imaging (HR-MR imaging) and DSA. However, very few stud- ter, vessel area (VA), and lumen area (LA) at the MLN or reference ies have explored the direct relationship between plaque distribution site were manually evaluated. Reference sites were defined accord- and postoperative complications after endovascular treatment from ing to Warfarin versus Aspirin for Symptomatic Intracranial the axial and coronal positions for basilar artery stenosis. The cur- Disease (WASID) trial as normal segments proximal to the steno- rent study investigated the distribution of basilar artery atheroscler- sis or distal vessels if the proximal segment was diseased. otic plaques and their clinical relevance using HR-MR imaging and On the basis of HR-MR imaging and DSA, we observed the DSA. Our findings can help neurointerventionalists with better following vessel parameters: patient selection and, thus, lower the procedural risk. � Wall area (WA): difference between VA and LA (VA – LA). � Plaque burden: [(WA – WA )/ VA ]  100%. MLN reference MLN MATERIALS AND METHODS � Remodeling index: VA MLN/VA reference. Subjects This study was based on the Clinical Registration Trial of Intracranial Stenosis degree is (1-Luminal Diameter at MLN/Luminal Stenting for Patients with Symptomatic Intracranial Artery Stenosis Diameter at the Reference Site) 100% from DSA. (CRTICAS) data base (ClinicalTrials.gov identifier: NCT01994161). Using 2 perpendicular lines, we divided the cross-sectional pla- The protocol complies with ethics principles of the Declaration of que into 4 quadrants at the MLN: ventral, dorsal, left, and right. Helsinki and good clinical practice and has been approved by the The left and right sites were classified as lateral sites. If the plaque the review board and ethic committee of Xuanwu Hospital, Capital was large and its thickest aspect spanned more than 2 quadrants, it Medical University ([2013] 004). Written informed consent was was considered distributed between .2quadrants (Fig 1A). In the obtained from all the patients. The results of this study have been coronal position, DSA was used to divide the basilar artery into 2 reported in accordance with the Strengthening The Reporting Of segments on the basis of the branches of the anterior-inferior cere- 15 18 Cohort Studies in Surgery (STROCSS) criteria. bellar artery. Lesions crossing the anterior-inferior cerebellar ar- The study included patients with basilar artery stenosis who tery were categorized as junctional segment lesions (Fig 1B). were enrolled between December 2013 and December 2015 in several high-volume tertiary centers in China. The inclusion cri- Interventional Procedure and Assessment of Outcome teria were as follows: 1) degree of stenosis of .70% as confirmed All patients were treated by a team of neurosurgeons and neuro- by DSA; 2) patients with basilar artery atherosclerotic stenosis radiologists with extensive experience in endovascular treatment. who experienced ischemic symptoms, such as dizziness, vertigo, Experienced operators determined the therapeutic strategy headache, double vision, slurred speech, and numbness or according to the lesion characteristics. Aspirin, 100 mg daily, was AJNR Am J Neuroradiol 44:530–35 May 2023 www.ajnr.org 531 Table 1: Clinical and lesion characteristics Variables All Patients (n = 140) Ischemic Events (n = 16) Nonischemic Events (n = 124) P Value Sex, male 106 (75.7%) 12 (75.0%) 87 (70.2%) .914 Age (mean) (yr) 61.9 (SD, 7.7) 62.5 (SD, 6.6) 61.8 (SD, 7.9) .728 BMI (mean) (kg/m ) 26.2 (SD, 3.0) 25.8 (SD, 2.2) 26.3 (SD, 3.1) .522 Qualifying event .419 TIA 23 (16.4%) 1 (6.3%) 22 (17.7%) Stroke 117 (83.6%) 15 (93.7%) 102 (82.3%) Hypertension 117 (83.6%) 14 (87.5%) 103 (83.1%) .927 Diabetes mellitus 58 (41.4%) 7 (43.8%) 51 (41.1%) .841 Hyperlipidemia 36 (25.7%) 4 (25.0%) 32 (25.8%) 1.000 CAD 14 (10.0%) 2 (12.5%) 12 (9.7%) 1.000 Smoking history 58 (41.4%) 6 (37.5%) 52 (41.9%) .735 Drinking history 38 (27.1%) 3 (18.8%) 35 (28.2%) .615 Preoperative mRS .218 ,2 125 (89.3%) 16 (100%) 109 (87.9%) $2 15 (10.7%) 0 15 (12.1%) Stenosis degree (mean) (%) 77.7 (SD, 9.3) 76.2 (SD, 14.2) 77.9 (SD, 9.2) .826 Plaque length (mean) (mm) 5.9 (SD, 3.8) 4.9 (SD, 3.2) 5.9 (SD, 3.9) .212 Plaque burden (mean) (%) 5.5 (SD, 23.6) 19.3 (SD, 18.3) 3.7 (SD, 23.6) .047 Remodeling index (mean) 0.8 (SD, 0.4) 0.9 (SD, 0.4) 0.8 (SD, 0.4) .430 Treatment type .323 PA 26 (18.6%) 5 (31.3%) 21 (16.9%) BMS 30 (21.4%) 2 (12.5%) 28 (22.6%) SES 84 (60.0%) 9 (56.2%) 75 (60.5%) Note:—BMI indicates body mass index; CAD, coronary artery disease; PA, primary angioplasty; BMS, balloon-mounted stent; SES, self-expansion stent. combined with clopidogrel, 75 mg daily for 5 days before, or a The average age of these patients was 61.9 (SD, 7.7) years. loading dose of aspirin and clopidogrel, 300 mg each, was used 1 Twenty-six (18.5%) patients underwent primary angioplasty, and 114 (81.5%) underwent stent placement, which included 30 bal- day before endovascular treatment. Standard protocols for the loon-mounted stents and 84 self-expansion stents. Furthermore, procedure were followed as described previously. Three-month 16 patients with postoperative ischemic events, including 3 TIAs, dual-antiplatelet therapy, comprising aspirin, 100 mg daily, and 4 perforating infarctions, 7 artery-to-artery embolisms, and 2 clopidogrel, 75 mg daily, was initiated following the intervention. mixed mechanisms were regarded as the ischemic events group, An experienced team of neurosurgeons and neuroradiologists and 124 patients without postoperative ischemic events, as the investigated the postoperative ischemic events, including TIA nonischemic events group (Online Supplemental Data). Table 1 and ischemic stroke. Ischemic stroke was defined as a neurologic summarizes the clinical and lesion characteristics, with the excep- deficit lasting .24 hours. TIA was defined as a neurologic deficit tion of plaque burden (mean, 19.3% [SD, 18.3%] versus 3.7% [SD, lasting ,24 hours. Depending on whether postoperative out- 23.6%]; P ¼ .047) between the ischemic events group and the non- come events occurred after endovascular treatment, patients were ischemic events group. classified into an either ischemic or nonischemic events group. A total of 140 basilar artery plaques were reviewed from the axial and coronal positions. In the axial view at the MLN site, Statistical Analysis 12.9% of plaques were distributed ventral to the basilar artery Data were analyzed using the SAS software (Version 9.4; SAS wall, and 22.1% in the lateral, 34.3% in the dorsal, and 30.7% in Institute). Quantitative variables are presented as means. Qualitative $2 quadrants. The plaques distributed in the lateral wall were variables are presented as numbers and percentages. Descriptive more common in the ischemic events group than in the nonis- analyses were performed for participants in the postoperative ische- chemic events group (43.8% versus 19.3%, P ¼ .049). In the coro- mic and nonischemic events group. The x test or Fisher exact test nal view, plaque distribution was most common at the segment was used to compare the categoric variables, as appropriate. The distal to the anterior-inferior cerebellar artery (60.7%), followed Student t test or Wilcoxon test was used to compare the quantitative by the segment proximal to the anterior-inferior cerebellar artery variables. Univariate and multivariate regression analyses were per- (35.0%), and least in the junctional segment (4.3%). Plaques dis- formed to investigate the factors influencing the postoperative ische- tributed at the junctional segment in the ischemic events group mic events. Variables with P, .1, along with sex, age, and treatment were more frequent compared with the nonischemic events type, were included in the multivariate regression analysis. P, .05 group (18.8% versus 2.4%, P ¼ .020). The additional details of was considered as statistically significant. plaque distribution are presented in Table 2. The risk of ischemic events was the highest in patients with plaques located at the lat- RESULTS eral wall (22.5%) and junctional segment (50.0%) of the basilar In total, 281 consecutive patients with severe symptomatic basilar artery (Online Supplemental Data). Additionally, the high risk of artery stenosis underwent endovascular treatment. Among them, ischemic events in patients with plaques located at the junctional 140 patients having complete HR-MR imaging and DSA data segment of the basilar artery was associated with a large remodel- were finally included in the analysis (Online Supplemental Data). ing index compared with that in the nonischemic events group 532 Luo May 2023 www.ajnr.org Table 2: Plaque distribution of the basilar artery explain the high risk associated with All Patients Ischemic Events Nonischemic Events endovascular treatment. Previous stud- Plaque Distribution (n = 140) (n = 16) (n = 124) P Value ies have suggested that SAMMPRIS, Axial position strict patient selection, technical devel- Ventral 18 (12.9%) 2 (12.5%) 16 (12.9%) 1.000 opment, and incremental experience of Lateral 31 (22.1%) 7 (43.8%) 24 (19.3%) .049 the operators reduces the risk of post- Dorsal 48 (34.3%) 3 (18.7%) 45 (36.3%) .262 operative complications for endovascu- $2 quadrants 43 (30.7%) 4 (25.0%) 39 (31.5%) .776 Coronal position lar treatment. Our study showed a Proximal segment 49 (35.0%) 6 (37.5%) 43 (34.7%) 1.000 relatively lower risk compared with Distal segment 85 (60.7%) 7 (43.8%) 78 (62.9%) .176 SAMMPRIS (21.6%) and is comparable Junctional segment 6 (4.3%) 3 (18.8%) 3 (2.4%) .020 27,28 with several studies (11.2%–14.2%). However, the prevention of postopera- tive complications is necessary to maxi- Table 3: Relationship between plaque distribution and ischemic mize the benefits of endovascular treatment. events by multivariate analysis It is highly likely that postoperative complications can be OR (95% CI) P Value reduced by assessing the plaque distribution and features. Plaque Age 1.00 (0.92–1.08) .997 distribution has been abundantly indicated to be a significant indi- Treatment type 0.99 (0.50–1.99) .994 cator of postoperative complications, thus revealing that postoper- Plaque burden 1.03 (1.01–1.06) .042 ative complications of intracranial atherosclerotic plaques located Plaque distribution in the posterior circulation were higher than those in the anterior Lateral 4.00 (1.21–13.23) .023 29-31 Junctional segment 8.75 (1.16–66.22) .036 circulation (12.1% versus 6.6, P, .01). However, the associa- tion of local distribution of basilar artery atherosclerotic plaques with postoperative complications is unclear. Several researchers (mean, 1.38 [SD, 0.20] versus 0.82 [SD, 0.29]; 95% CI, 0.05–1.13; have hypothesized that plaques near the perforating orifices might P ¼ .049) (Online Supplemental Data). be a determinant of postoperative complications through narrative The multivariate logistic regression analysis showed that pla- 6,18,32,33 analysis in plaque microanatomy studies. ques distributed at the lateral wall (OR ¼ 4.00; 95% CI, 1.21– In this study, plaques present in the lateral wall were associated 13.23; P ¼ .023) and junctional segments (OR ¼ 8.75; 95% CI, with a higher risk of postoperative complications. Penetrating 1.16–66.22; P ¼ .036) aswell asplaque burden (OR ¼ 1.03; 95% arteries from the lateral and dorsal sides of the basilar artery have CI, 1.01–1.06; P ¼ .042) were associated with a higher risk of been observed in previous studies. According to the anatomic postoperative ischemic events (Table 3, Fig 2). studies, 65.3% of penetrating arteries originate from the lateral side of the basilar artery, whereas 34.7% originate from the dorsal DISCUSSION side. Additionally, the anastomosis rate of penetrating arteries In this study, symptomatic patients with severe basilar artery ste- emerging from the basilar artery is high (range, 41.6%–66.6%). nosis were enrolled to investigate the correlation of atherosclerotic From an axial perspective, the anastomosis rate of penetrations plaque distribution with postoperative complications. The risk of emerging from the dorsal side was higher than that on the lateral postoperative ischemic events in patients with severe symptomatic side. Moreover, 99% of the anastomoses of penetrating arteries basilar artery stenosis was 11.4% (16/140). Although plaque distri- from thedorsal sideof basilar artery arelocated on theventral sur- bution of the basilar artery was most commonly observed at the face of the pontocerebrum surface, 57.5% of the anastomoses occur dorsal wall of the basilar artery in the axial (34.3%) and distal seg- between the penetrating arteries of the pontocerebrum, and 21.3%, ments in the coronal view (60.7%), the risk of postoperative com- between penetrations originating from the basilar artery and ante- plications was highest when the plaques were situated in the rior-inferior cerebellar artery. As a result, plaques involving the lateral wall and junctional segment of the basilar artery. In addi- lateral side of the basilar artery may be a risk factor for endovascu- tion to the large plaque burden, plaques located at the lateral wall lar treatment for patients with severe basilar artery stenosis. and junctional segment of the basilar artery were independent risk In addition, a large plaque burden is associated with postopera- factors for postoperative ischemic events. tive complications, which may be due to a large plaque burden The high risk of postoperative complications is a substantial being more vulnerable during the expansion process of the balloon limitation for endovascular treatment of intracranial atheroscler- or stent. Furthermore, a large plaque burden has a high risk of 4,20 otic stenosis, especially in the posterior circulation. The basilar initial and recurrent ischemic symptoms in patients with intracra- 38-40 artery is the main artery for the posterior circulation, which has nial stenosis. Thus, anevaluationof bothplaque burden and the highest risk of postoperative complications for endovascular distribution characteristics may be helpful in excluding high-risk treatment among the intracranial arteries. The posterior circula- patients from endovascular treatment of basilar artery stenosis. tion appears to be more capable of plaque burden because it has a This study has some limitations. First, although the study cohort lower blood flow and less sympathetic innervation compared had a larger sample size compared with other HR-MR imaging 21-24 with the anterior circulation. Additionally, the number of studies, the incidence of postoperative complications was low, com- 17, 41 perforating arteries in the basilar artery is significantly higher prising only 16 cases. Therefore, the impact of plaque location than that of the other intracranial arteries. 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Clinical Relevance of Plaque Distribution for Basilar Artery Stenosis

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American Journal of Neuroradiology
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© 2023 by American Journal of Neuroradiology. Indicates open access to non-subscribers at www.ajnr.org
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Clinical Relevance of Plaque Distribution for Basilar Artery Stenosis J. Luo, X. Bai, K. Huang, T. Wang, R. Yang, L. Li, Q. Tian, R. Xu, T. Li, Y. Wang, Y. Chen, P. Gao, J. Chen, B. Yang, Y. Ma and L. Jiao AJNR Am J Neuroradiol 2023, 44 (5) 530-535 This information is current as doi: https://doi.org/10.3174/ajnr.A7839 of June 3, 2023. http://www.ajnr.org/content/44/5/530 ORIGINAL RESEARCH ADULT BRAIN Clinical Relevance of Plaque Distribution for Basilar Artery Stenosis J. Luo, X. Bai, K. Huang, T. Wang, R. Yang, L. Li, Q. Tian, R. Xu, T. Li, Y. Wang, Y. Chen, P. Gao, J. Chen, B. Yang, Y. Ma, and L. Jiao ABSTRACT BACKGROUND AND PURPOSE: There is no clear association between plaque distribution and postoperative complications in patients with basilar artery atherosclerotic stenosis. The aim of this study was to determine whether plaque distribution and post- operative complications after endovascular treatment for basilar artery stenosis are related. MATERIALS AND METHODS: Our study enrolled patients with severe basilar artery stenosis who were scanned with high-resolution MR imaging and followed by DSA before the intervention. According to high-resolution MR imaging, plaques can be classified as ven- tral, lateral, dorsal, or involved in 2 quadrants. Plaques affecting the proximal, distal, or junctional segments of the basilar artery were classified according to DSA. An experienced independent team assessed ischemic events after the intervention using MR imaging. Further analysis was conducted to determine the relationship between plaque distribution and postoperative complications. RESULTS: A total of 140 eligible patients were included in the study, with a postoperative complication rate of 11.4%. These patients were an average age of 61.9 (SD, 7.7) years. Dorsal wall plaques accounted for 34.3% of all plaques, and plaques distal to the ante- rior-inferior cerebellar artery accounted for 60.7%. Postoperative complications of endovascular treatment were associated with plaques located at the lateral wall (OR ¼ 4.00; 95% CI, 1.21–13.23; P ¼ .023), junctional segment (OR ¼ 8.75; 95% CI, 1.16–66.22; P ¼ .036), and plaque burden (OR ¼ 1.03; 95% CI, 1.01–1.06; P ¼ .042). CONCLUSIONS: Plaques with a large burden located at the junctional segment and lateral wall of the basilar artery may increase the likelihood of postoperative complications following endovascular therapy. A larger sample size is needed for future studies. ABBREVIATIONS: HR-MR imaging ¼ high-resolution MR imaging; LA ¼ lumen area; MLN ¼ maximal lumen narrowing; VA ¼ vessel area; WA ¼ wall area he basilar artery is the main artery for the posterior intracra- Patients with symptomatic and severe basilar artery stenosis Tnial circulation, where atherosclerotic stenosis is frequently ($70%) may benefit from endovascular treatment, including discovered in patients with ischemic events, such as stroke and primary angiography, balloon-mounted stent placement, and 1 2 TIA, which are responsible for 10.7% of strokes annually. self-expanding stent placement. Compared with the those in the anterior circulation, postoperative complications are higher in the posterior circulation with a reported risk of 21.6% in the Received November 20, 2022; accepted after revision March 1, 2023. 3,4 basilar artery. Therefore, it is crucial to understand and pre- From the China International Neuroscience Institute (J.L., X.B., T.W., R.Y., L.L., R.X., T.L., Y.W., Y.C., P.G., J.C., B.Y., Y.M., L.J.), Beijing, China; Department of Neurosurgery vent a high risk of complications occurring during endovascular (J.L., X.B., T.W., R.Y., L.L., R.X., T.L., Y.W., Y.C., P.G., J.C., B.Y., Y.M., L.J.), Xuanwu treatment in patients with basilar artery stenosis. Hospital, Beijing Key Laboratory of Clinical Epidemiology (Q.T.), School of Public Health, and Department of Interventional Radiology (P.G., L.J.), Xuanwu Hospital, The distribution of atherosclerotic plaques is associated with Capital Medical University, Beijing, China; and The Eighth Affiliated Hospital (K.H.), 5-7 the risk of ischemic events. For example, it is more likely that SUN YAT-SEN University, Shenzhen, Guangdong Province, China. atherosclerotic plaques located near perforating orifices are symp- This study was funded by the National Key Research and Development Program of China (2016YFC1301703), Beijing Science and Technology Planning Project tomatic during stent placement and may have a “snow plowing” (Z201100005520019), and Beijing Hospitals Authority's Ascent Plan (DFL20220702). effect. Several postmortem studies have demonstrated that basilar Please address correspondence to Liqun Jiao, MD, PhD, Departments of artery perforators typically originate from the lateral and dorsal Neurosurgery and Interventional Radiology, Xuanwu Hospital, Capital Medical University, No. 45 Changchun St, Xicheng District, 100053, Beijing, China; walls of the segment, distal from the anterior-inferior cerebellar e-mail: liqunjiao@sina.cn artery, possibly explaining the high rate of postoperative compli- Indicates open access to non-subscribers at www.ajnr.org 9,10 cations. However, the relationship between the distribution of basilar artery plaque and postoperative complications has not yet Indicates article with online supplemental data. http://dx.doi.org/10.3174/ajnr.A7839 been reported . 530 Luo May 2023 www.ajnr.org weakness; 3) treatment using endovascular therapy; 4) HR-MR imaging performed before the intervention; and 5) MR imaging performed before and within 72 hours after the intervention. The exclusion criteria were as follows: 1) stroke caused by occlu- sion of the basilar artery, 2) concurrent endovascular treatment of another intracranial or extracranial vessel, 3) basilar artery ste- nosis accompanied by moderate-to-severe vertebral artery stenosis, and 4) nonatherosclerotic causes (eg, Moyamoya disease, vasculitis, or dissection). Imaging Protocols and Evaluation FIG 1. A, The basilar artery is divided into 4 quadrants at the axial Before the intervention, all eligible patients were examined position based on high-resolution MR imaging. B, The basilar artery is using a 3T MR imaging scanner (Magnetom Spectra; Siemens) divided into 2 segments referring to the AICA on the basis of DSA, equipped with a standard 8-channel head coil. The scans were the proximal and distal segments. The junctional segment is defined when the plaque involves both segments across the anterior-inferior obtained using multiple sequences, including fast spin-echo T1- cerebellar artery. weighted imaging, TOF-MR angiography, and T1-weighted enhanced imaging. The parameters of the sequences are Understanding the distribution of basilar artery plaques can described in the Online Supplemental Data. HR-MR imaging help in reducing the incidence of postoperative complications. was acquired in the sagittal plane covering the basilar artery ves- Evidence from studies since the Stenting versus Aggressive Medical sel. Reconstruction of the axial, coronal, and sagittal views was Management for Preventing Recurrent Stroke in Intracranial required to analyze all the images. DSA examinations were also Stenosis (SAMMPRIS) trial has shown that the postoperative risk of performed for all the eligible patients. endovascular treatment for intracranial stenosis can be reduced An image core lab (http://imagecorelabcn.com/)was used to from 14.7% to 9.4% by excluding symptomatic patients with perfo- review all the images. The clinical data of patients were undisclosed rating infarction. The postoperative risk could be reduced exclud- and not included in the statistical analyses. Before the formal ing perforating infarction actually infers the plaque location, assessment, 5% of data from the analyzed cohort was used to train whether it is near perforating orifices, according to the phenotype of raters. Whenever the agreement was excellent (reliability, .0.75) cerebral infarction. Presently, plaque distribution in axial and coro- between 2 raters, the imaging data were formally evaluated. The nal positions can be precisely evaluated using high-resolution MR maximal lumen narrowing (MLN) or reference site, lumen diame- 12,13 imaging (HR-MR imaging) and DSA. However, very few stud- ter, vessel area (VA), and lumen area (LA) at the MLN or reference ies have explored the direct relationship between plaque distribution site were manually evaluated. Reference sites were defined accord- and postoperative complications after endovascular treatment from ing to Warfarin versus Aspirin for Symptomatic Intracranial the axial and coronal positions for basilar artery stenosis. The cur- Disease (WASID) trial as normal segments proximal to the steno- rent study investigated the distribution of basilar artery atheroscler- sis or distal vessels if the proximal segment was diseased. otic plaques and their clinical relevance using HR-MR imaging and On the basis of HR-MR imaging and DSA, we observed the DSA. Our findings can help neurointerventionalists with better following vessel parameters: patient selection and, thus, lower the procedural risk. � Wall area (WA): difference between VA and LA (VA – LA). � Plaque burden: [(WA – WA )/ VA ]  100%. MLN reference MLN MATERIALS AND METHODS � Remodeling index: VA MLN/VA reference. Subjects This study was based on the Clinical Registration Trial of Intracranial Stenosis degree is (1-Luminal Diameter at MLN/Luminal Stenting for Patients with Symptomatic Intracranial Artery Stenosis Diameter at the Reference Site) 100% from DSA. (CRTICAS) data base (ClinicalTrials.gov identifier: NCT01994161). Using 2 perpendicular lines, we divided the cross-sectional pla- The protocol complies with ethics principles of the Declaration of que into 4 quadrants at the MLN: ventral, dorsal, left, and right. Helsinki and good clinical practice and has been approved by the The left and right sites were classified as lateral sites. If the plaque the review board and ethic committee of Xuanwu Hospital, Capital was large and its thickest aspect spanned more than 2 quadrants, it Medical University ([2013] 004). Written informed consent was was considered distributed between .2quadrants (Fig 1A). In the obtained from all the patients. The results of this study have been coronal position, DSA was used to divide the basilar artery into 2 reported in accordance with the Strengthening The Reporting Of segments on the basis of the branches of the anterior-inferior cere- 15 18 Cohort Studies in Surgery (STROCSS) criteria. bellar artery. Lesions crossing the anterior-inferior cerebellar ar- The study included patients with basilar artery stenosis who tery were categorized as junctional segment lesions (Fig 1B). were enrolled between December 2013 and December 2015 in several high-volume tertiary centers in China. The inclusion cri- Interventional Procedure and Assessment of Outcome teria were as follows: 1) degree of stenosis of .70% as confirmed All patients were treated by a team of neurosurgeons and neuro- by DSA; 2) patients with basilar artery atherosclerotic stenosis radiologists with extensive experience in endovascular treatment. who experienced ischemic symptoms, such as dizziness, vertigo, Experienced operators determined the therapeutic strategy headache, double vision, slurred speech, and numbness or according to the lesion characteristics. Aspirin, 100 mg daily, was AJNR Am J Neuroradiol 44:530–35 May 2023 www.ajnr.org 531 Table 1: Clinical and lesion characteristics Variables All Patients (n = 140) Ischemic Events (n = 16) Nonischemic Events (n = 124) P Value Sex, male 106 (75.7%) 12 (75.0%) 87 (70.2%) .914 Age (mean) (yr) 61.9 (SD, 7.7) 62.5 (SD, 6.6) 61.8 (SD, 7.9) .728 BMI (mean) (kg/m ) 26.2 (SD, 3.0) 25.8 (SD, 2.2) 26.3 (SD, 3.1) .522 Qualifying event .419 TIA 23 (16.4%) 1 (6.3%) 22 (17.7%) Stroke 117 (83.6%) 15 (93.7%) 102 (82.3%) Hypertension 117 (83.6%) 14 (87.5%) 103 (83.1%) .927 Diabetes mellitus 58 (41.4%) 7 (43.8%) 51 (41.1%) .841 Hyperlipidemia 36 (25.7%) 4 (25.0%) 32 (25.8%) 1.000 CAD 14 (10.0%) 2 (12.5%) 12 (9.7%) 1.000 Smoking history 58 (41.4%) 6 (37.5%) 52 (41.9%) .735 Drinking history 38 (27.1%) 3 (18.8%) 35 (28.2%) .615 Preoperative mRS .218 ,2 125 (89.3%) 16 (100%) 109 (87.9%) $2 15 (10.7%) 0 15 (12.1%) Stenosis degree (mean) (%) 77.7 (SD, 9.3) 76.2 (SD, 14.2) 77.9 (SD, 9.2) .826 Plaque length (mean) (mm) 5.9 (SD, 3.8) 4.9 (SD, 3.2) 5.9 (SD, 3.9) .212 Plaque burden (mean) (%) 5.5 (SD, 23.6) 19.3 (SD, 18.3) 3.7 (SD, 23.6) .047 Remodeling index (mean) 0.8 (SD, 0.4) 0.9 (SD, 0.4) 0.8 (SD, 0.4) .430 Treatment type .323 PA 26 (18.6%) 5 (31.3%) 21 (16.9%) BMS 30 (21.4%) 2 (12.5%) 28 (22.6%) SES 84 (60.0%) 9 (56.2%) 75 (60.5%) Note:—BMI indicates body mass index; CAD, coronary artery disease; PA, primary angioplasty; BMS, balloon-mounted stent; SES, self-expansion stent. combined with clopidogrel, 75 mg daily for 5 days before, or a The average age of these patients was 61.9 (SD, 7.7) years. loading dose of aspirin and clopidogrel, 300 mg each, was used 1 Twenty-six (18.5%) patients underwent primary angioplasty, and 114 (81.5%) underwent stent placement, which included 30 bal- day before endovascular treatment. Standard protocols for the loon-mounted stents and 84 self-expansion stents. Furthermore, procedure were followed as described previously. Three-month 16 patients with postoperative ischemic events, including 3 TIAs, dual-antiplatelet therapy, comprising aspirin, 100 mg daily, and 4 perforating infarctions, 7 artery-to-artery embolisms, and 2 clopidogrel, 75 mg daily, was initiated following the intervention. mixed mechanisms were regarded as the ischemic events group, An experienced team of neurosurgeons and neuroradiologists and 124 patients without postoperative ischemic events, as the investigated the postoperative ischemic events, including TIA nonischemic events group (Online Supplemental Data). Table 1 and ischemic stroke. Ischemic stroke was defined as a neurologic summarizes the clinical and lesion characteristics, with the excep- deficit lasting .24 hours. TIA was defined as a neurologic deficit tion of plaque burden (mean, 19.3% [SD, 18.3%] versus 3.7% [SD, lasting ,24 hours. Depending on whether postoperative out- 23.6%]; P ¼ .047) between the ischemic events group and the non- come events occurred after endovascular treatment, patients were ischemic events group. classified into an either ischemic or nonischemic events group. A total of 140 basilar artery plaques were reviewed from the axial and coronal positions. In the axial view at the MLN site, Statistical Analysis 12.9% of plaques were distributed ventral to the basilar artery Data were analyzed using the SAS software (Version 9.4; SAS wall, and 22.1% in the lateral, 34.3% in the dorsal, and 30.7% in Institute). Quantitative variables are presented as means. Qualitative $2 quadrants. The plaques distributed in the lateral wall were variables are presented as numbers and percentages. Descriptive more common in the ischemic events group than in the nonis- analyses were performed for participants in the postoperative ische- chemic events group (43.8% versus 19.3%, P ¼ .049). In the coro- mic and nonischemic events group. The x test or Fisher exact test nal view, plaque distribution was most common at the segment was used to compare the categoric variables, as appropriate. The distal to the anterior-inferior cerebellar artery (60.7%), followed Student t test or Wilcoxon test was used to compare the quantitative by the segment proximal to the anterior-inferior cerebellar artery variables. Univariate and multivariate regression analyses were per- (35.0%), and least in the junctional segment (4.3%). Plaques dis- formed to investigate the factors influencing the postoperative ische- tributed at the junctional segment in the ischemic events group mic events. Variables with P, .1, along with sex, age, and treatment were more frequent compared with the nonischemic events type, were included in the multivariate regression analysis. P, .05 group (18.8% versus 2.4%, P ¼ .020). The additional details of was considered as statistically significant. plaque distribution are presented in Table 2. The risk of ischemic events was the highest in patients with plaques located at the lat- RESULTS eral wall (22.5%) and junctional segment (50.0%) of the basilar In total, 281 consecutive patients with severe symptomatic basilar artery (Online Supplemental Data). Additionally, the high risk of artery stenosis underwent endovascular treatment. Among them, ischemic events in patients with plaques located at the junctional 140 patients having complete HR-MR imaging and DSA data segment of the basilar artery was associated with a large remodel- were finally included in the analysis (Online Supplemental Data). ing index compared with that in the nonischemic events group 532 Luo May 2023 www.ajnr.org Table 2: Plaque distribution of the basilar artery explain the high risk associated with All Patients Ischemic Events Nonischemic Events endovascular treatment. Previous stud- Plaque Distribution (n = 140) (n = 16) (n = 124) P Value ies have suggested that SAMMPRIS, Axial position strict patient selection, technical devel- Ventral 18 (12.9%) 2 (12.5%) 16 (12.9%) 1.000 opment, and incremental experience of Lateral 31 (22.1%) 7 (43.8%) 24 (19.3%) .049 the operators reduces the risk of post- Dorsal 48 (34.3%) 3 (18.7%) 45 (36.3%) .262 operative complications for endovascu- $2 quadrants 43 (30.7%) 4 (25.0%) 39 (31.5%) .776 Coronal position lar treatment. Our study showed a Proximal segment 49 (35.0%) 6 (37.5%) 43 (34.7%) 1.000 relatively lower risk compared with Distal segment 85 (60.7%) 7 (43.8%) 78 (62.9%) .176 SAMMPRIS (21.6%) and is comparable Junctional segment 6 (4.3%) 3 (18.8%) 3 (2.4%) .020 27,28 with several studies (11.2%–14.2%). However, the prevention of postopera- tive complications is necessary to maxi- Table 3: Relationship between plaque distribution and ischemic mize the benefits of endovascular treatment. events by multivariate analysis It is highly likely that postoperative complications can be OR (95% CI) P Value reduced by assessing the plaque distribution and features. Plaque Age 1.00 (0.92–1.08) .997 distribution has been abundantly indicated to be a significant indi- Treatment type 0.99 (0.50–1.99) .994 cator of postoperative complications, thus revealing that postoper- Plaque burden 1.03 (1.01–1.06) .042 ative complications of intracranial atherosclerotic plaques located Plaque distribution in the posterior circulation were higher than those in the anterior Lateral 4.00 (1.21–13.23) .023 29-31 Junctional segment 8.75 (1.16–66.22) .036 circulation (12.1% versus 6.6, P, .01). However, the associa- tion of local distribution of basilar artery atherosclerotic plaques with postoperative complications is unclear. Several researchers (mean, 1.38 [SD, 0.20] versus 0.82 [SD, 0.29]; 95% CI, 0.05–1.13; have hypothesized that plaques near the perforating orifices might P ¼ .049) (Online Supplemental Data). be a determinant of postoperative complications through narrative The multivariate logistic regression analysis showed that pla- 6,18,32,33 analysis in plaque microanatomy studies. ques distributed at the lateral wall (OR ¼ 4.00; 95% CI, 1.21– In this study, plaques present in the lateral wall were associated 13.23; P ¼ .023) and junctional segments (OR ¼ 8.75; 95% CI, with a higher risk of postoperative complications. Penetrating 1.16–66.22; P ¼ .036) aswell asplaque burden (OR ¼ 1.03; 95% arteries from the lateral and dorsal sides of the basilar artery have CI, 1.01–1.06; P ¼ .042) were associated with a higher risk of been observed in previous studies. According to the anatomic postoperative ischemic events (Table 3, Fig 2). studies, 65.3% of penetrating arteries originate from the lateral side of the basilar artery, whereas 34.7% originate from the dorsal DISCUSSION side. Additionally, the anastomosis rate of penetrating arteries In this study, symptomatic patients with severe basilar artery ste- emerging from the basilar artery is high (range, 41.6%–66.6%). nosis were enrolled to investigate the correlation of atherosclerotic From an axial perspective, the anastomosis rate of penetrations plaque distribution with postoperative complications. The risk of emerging from the dorsal side was higher than that on the lateral postoperative ischemic events in patients with severe symptomatic side. Moreover, 99% of the anastomoses of penetrating arteries basilar artery stenosis was 11.4% (16/140). Although plaque distri- from thedorsal sideof basilar artery arelocated on theventral sur- bution of the basilar artery was most commonly observed at the face of the pontocerebrum surface, 57.5% of the anastomoses occur dorsal wall of the basilar artery in the axial (34.3%) and distal seg- between the penetrating arteries of the pontocerebrum, and 21.3%, ments in the coronal view (60.7%), the risk of postoperative com- between penetrations originating from the basilar artery and ante- plications was highest when the plaques were situated in the rior-inferior cerebellar artery. As a result, plaques involving the lateral wall and junctional segment of the basilar artery. In addi- lateral side of the basilar artery may be a risk factor for endovascu- tion to the large plaque burden, plaques located at the lateral wall lar treatment for patients with severe basilar artery stenosis. and junctional segment of the basilar artery were independent risk In addition, a large plaque burden is associated with postopera- factors for postoperative ischemic events. tive complications, which may be due to a large plaque burden The high risk of postoperative complications is a substantial being more vulnerable during the expansion process of the balloon limitation for endovascular treatment of intracranial atheroscler- or stent. Furthermore, a large plaque burden has a high risk of 4,20 otic stenosis, especially in the posterior circulation. The basilar initial and recurrent ischemic symptoms in patients with intracra- 38-40 artery is the main artery for the posterior circulation, which has nial stenosis. Thus, anevaluationof bothplaque burden and the highest risk of postoperative complications for endovascular distribution characteristics may be helpful in excluding high-risk treatment among the intracranial arteries. The posterior circula- patients from endovascular treatment of basilar artery stenosis. tion appears to be more capable of plaque burden because it has a This study has some limitations. First, although the study cohort lower blood flow and less sympathetic innervation compared had a larger sample size compared with other HR-MR imaging 21-24 with the anterior circulation. Additionally, the number of studies, the incidence of postoperative complications was low, com- 17, 41 perforating arteries in the basilar artery is significantly higher prising only 16 cases. Therefore, the impact of plaque location than that of the other intracranial arteries. 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Journal

American Journal of Neuroradiology – American Journal of Neuroradiology

Published: May 1, 2023

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