
Chinese Journal of Stroke ›› 2025, Vol. 20 ›› Issue (4): 500-510.DOI: 10.3969/j.issn.1673-5765.2025.04.015
Previous Articles Next Articles
ZHAO Kaijie1,2, SUN Xiuting1,2, YUAN Man1,2, HU Wanzhen2, ZHANG Xiaoyan2
Received:2024-03-26
Online:2025-04-20
Published:2025-04-20
Contact:
ZHANG Xiaoyan, E-mail: zhangxiaoyan060110@163.com
赵开杰1,2,孙秀亭1,2,袁曼1,2,胡婉贞2,张晓燕2
通讯作者:
张晓燕 zhangxiaoyan060110@163.com
CLC Number:
ZHAO Kaijie, SUN Xiuting, YUAN Man, HU Wanzhen, ZHANG Xiaoyan. Advances in Cerebral Collateral Circulation Assessment Methods[J]. Chinese Journal of Stroke, 2025, 20(4): 500-510.
赵开杰, 孙秀亭, 袁曼, 胡婉贞, 张晓燕. 脑侧支循环评估方法的研究进展[J]. 中国卒中杂志, 2025, 20(4): 500-510.
| [1] SEIFERT K,HEIT J J. Collateral blood flow and ischemic core growth[J]. Transl Stroke Res,2023,14(1):13-21. [2] 中华医学会急诊医学分会,急性缺血性脑卒中侧支循环评估与干预中国急诊专家共识组. 急性缺血性脑卒中侧支循环评估与干预中国急诊专家共识[J]. 中华急诊医学杂志,2022,31(10):1310-1318. Chinese Society of Emergency Medicine,Chinese Emergency Expert Consensus Group on Collateral Circulation Assessment and Intervention in Acute Ischemic Stroke. Chinese emergency expert consensus on collateral circulation assessment and intervention in acute ischemic stroke[J]. Chin J Emerg Med,2022,31(10):1310-1318. [3] LIN L T,YANG J H,CHEN C S,et al. Association of collateral status and ischemic core growth in patients with acute ischemic stroke[J/OL]. Neurology,2021,96(2):e161-e170[2024-02-12]. https://doi.org/10.1212/WNL.0000000000011258. [4] CAPPELLARI M,SAIA V,PRACUCCI G,et al. Association of the careggi collateral score with radiological outcomes after thrombectomy for stroke with an occlusion of the middle cerebral artery[J]. J Thromb Thrombolysis,2022,54(2):309-317. [5] LEE J S,BANG O Y. Collateral status and outcomes after thrombectomy[J]. Transl Stroke Res,2023,14(1):22-37. [6] NAWABI J,KNIEP H,BROOCKS G,et al. Clinical relevance of asymptomatic intracerebral hemorrhage post thrombectomy depends on angiographic collateral score[J]. J Cereb Blood Flow Metab,2020,40(8):1599-1607. [7] LIU L P,XU A D,WONG L K,et al. Chinese consensus statement on the evaluation and intervention of collateral circulation for ischemic stroke[J]. CNS Neurosci Ther,2014,20(3):202-208. [8] KIM S J,NOH H J,YOON C W,et al. Multiphasic perfusion computed tomography as a predictor of collateral flow in acute ischemic stroke:comparison with digital subtraction angiography[J]. Eur Neurol,2012,67(4):252-255. [9] D’ANDREA A,CONTE M,CAVALLARO M,et al. Transcranial Doppler ultrasonography:from methodology to major clinical applications[J]. World J Cardiol,2016,8(7):383-400. [10] VAN DER HOEVEN E J,MCVERRY F,VOS J A,et al. Collateral flow predicts outcome after basilar artery occlusion:the posterior circulation collateral score[J]. Int J Stroke,2016,11(7):768-775. [11] 罗弦,楚兰,阮志兵,等. 多时相CTA对急性脑梗死的侧支循环及其预后的评价研究[J]. 医学影像学杂志,2020,30(11):1965-1969. LUO X,CHU L,RUAN Z B,et al. Evaluation of collateral circulation and prognosis of acute cerebral infarction with multi-phase CTA[J]. J Med Imaging,2020,30(11):1965-1969. [12] 李晗,王希明,郝光宇,等. 多期CTA与单期CTA评估急性缺血性脑卒中患者侧支状态的对照研究[J]. 临床放射学杂志,2020,39(12):2375-2379. LI H,WANG X M,HAO G Y,et al. Comparative study of multi-phase CTA and single-phase CTA in evaluating collateral status in patients with acute ischemic stroke[J]. Journal of Clinical Radiology,2020,39(12):2375-2379. [13] OSPEL J M,VOLNY O,QIU W,et al. Displaying multiphase CT angiography using a time-variant color map:practical considerations and potential applications in patients with acute stroke[J]. AJNR Am J Neuroradiol,2020,41(2):200-205. [14] MUEHLEN I,KLOSKA S P,GÖLITZ P,et al. Noninvasive collateral flow velocity imaging in acute ischemic stroke:intraindividual comparison of 4D-CT angiography with digital subtraction angiography[J]. Rofo,2019,191(9):827-835. [15] HOEFFNER E G,CASE I,JAIN R,et al. Cerebral perfusion CT:technique and clinical applications[J]. Radiology,2004,231(3):632-644. [16] TRILLO S,RAMOS M C,AGUIRRE C,et al. Assessment of collateral circulation using perfusion CT in middle cerebral artery thrombectomy-treated patients[J/OL]. J Stroke Cerebrovasc Dis,2020,29(7):104805[2024-02-12]. https://doi.org/10.1016/j.jstrokecerebrovasdis.2020.104805. [17] LIN L T,CHEN C S,TIAN H Q,et al. Perfusion computed tomography accurately quantifies collateral flow after acute ischemic stroke[J]. Stroke,2020,51(3):1006-1009. [18] NAEL K,SAKAI Y,LARSON J,et al. CT perfusion collateral index in assessment of collaterals in acute ischemic stroke with delayed presentation:comparison to single phase CTA[J]. J Neuroradiol,2022,49(2):198-204. [19] SCHREGEL K,TSOGKAS I,PETER C,et al. Outcome prediction using perfusion parameters and collateral scores of multi-phase and single-phase CT angiography in acute stroke:need for one,two,three,or thirty scans?[J]. J Stroke,2018,20(3):362-372. [20] MA Y C,CHEN A Q,GUO F,et al. The value of whole-brain CT perfusion imaging combined with dynamic CT angiography in the evaluation of pial collateral circulation with middle cerebral artery occlusion[J]. Technol Health Care,2022,30(4):967-979. [21] 朱杰,王浩,魏冉,等. 动态CTA结合CT灌注在软脑膜侧支循环评估中的运用[J]. 中国中西医结合影像学杂志,2021,19(4):325-329. ZHU J,WANG H,WEI R,et al. Application of dynamic CTA combined with CT perfusion in the evaluation of leptomeningeal collateral circulation[J]. Chinese Imaging Journal of Integrated Traditional and Western Medicine,2021,19(4):325-329. [22] LAU V I,JAIDKA A,WISKAR K,et al. Better with ultrasound:transcranial Doppler[J]. Chest,2020,157(1):142-150. [23] GUAN J X,ZHANG S F,ZHOU Q,et al. Usefulness of transcranial Doppler ultrasound in evaluating cervical-cranial collateral circulations[J]. Interv Neurol,2013,2(1):8-18. [24] HAKIMI R,ALEXANDROV A V,GARAMI Z. Neuro-ultrasonography[J]. Neurol Clin,2020,38(1):215-229. [25] FINNSDÓTTIR H,SZEGEDI I,OLÁH L,et al. The applications of transcranial Doppler in ischemic stroke[J]. Ideggyogy Sz,2020,73(11/12):367-378. [26] SPENCE J D. Uses of ultrasound in stroke prevention[J]. Cardiovasc Diagn Ther,2020,10(4):955-964. [27] ADIYAMAN D,ATAKUL B K,KUYUCU M,et al. Difference between near-field and far-field of middle cerebral artery Doppler pulsatility index and peak systolic velocity:a prospective study[J]. Clin Exp Obstet Gynecol,2021,48(1):66-72. [28] JAISWAL S K,FU-LING Y,GU L H,et al. Accuracy of transcranial Doppler ultrasound compared with magnetic resonance angiography in the diagnosis of intracranial artery stenosis[J]. J Neurosci Rural Pract,2019,10(3):400-404. [29] MOWLA A,SHAKIBAJAHROMI B,KABIR R,et al. Transcranial Doppler and magnetic resonance angiography assessment of intracranial stenosis:an analysis of screening modalities[J]. Brain Circ,2020,6(3):181-184. [30] TSUI B,NOUR M,CHEN I,et al. MR angiography in assessment of collaterals in patients with acute ischemic stroke:a comparative analysis with digital subtraction angiography[J/OL]. Brain Sci,2022,12(9):1181[2024-02-12]. https://doi.org/10.3390/brainsci12091181. [31] ZHOU Z E,MALAVERA A,YOSHIMURA S,et al. Clinical prognosis of FLAIR hyperintense arteries in ischaemic stroke patients:a systematic review and meta-analysis[J]. J Neurol Neurosurg Psychiatry,2020,91(5):475-482. [32] SUZUKI Y,FUJIMA N,VAN OSCH M J P. Intracranial 3D and 4D MR angiography using arterial spin labeling:technical considerations[J]. Magn Reson Med Sci,2020,19(4):294-309. [33] JANSEN I G H,VAN VUUREN A B,VAN ZWAM W H,et al. Absence of cortical vein opacification is associated with lack of intra-arterial therapy benefit in stroke[J]. Radiology,2018,286(2):643-650. [34] PRANEVICIUS M,PRANEVICIUS O. Cerebral venous steal:blood flow diversion with increased tissue pressure[J]. Neurosurgery,2002,51(5):1267-1274. [35] FAIZY T D,KABIRI R,CHRISTENSEN S,et al. Favorable venous outflow profiles correlate with favorable tissue-level collaterals and clinical outcome[J]. Stroke,2021,52(5):1761-1767. [36] WANG J J,LI J,LIU J Y,et al. Significant slowed cortical venous blood flow in patients with acute ischemic stroke with large vessel occlusion suggests poor collateral circulation and prognosis[J]. Acad Radiol,2023,30(9):1896-1903. [37] FAIZY T D,MLYNASH M,KABIRI R,et al. The cerebral collateral cascade:comprehensive blood flow in ischemic stroke[J/OL]. Neurology,2022,98(23):e2296-e2306[2024-02-12]. https://doi.org/10.1212/WNL.0000000000200340. [38] FAIZY T D,WINKELMEIER L,MLYNASH M,et al. Brain edema growth after thrombectomy is associated with comprehensive collateral blood flow[J]. J Neurointerv Surg,2024,16(12):1334-1340. [39] CONSOLI A,PIZZUTO S,SGRECCIA A,et al. Angiographic collateral venous phase:a novel landmark for leptomeningeal collaterals evaluation in acute ischemic stroke[J/OL]. J Neurointerv Surg,2023,15(e2):e323-e329[2024-02-12]. https://doi.org/10.1136/jnis-2022-019653. [40] KHAN A,DE BOEVER P,GERRITS N,et al. Retinal vessel multifractals predict pial collateral status in patients with acute ischemic stroke[J/OL]. PLoS One,2022,17(5):e0267837[2024-02-12]. https://doi.org/10.1371/journal.pone.0267837. [41] KHAN A,MENON A,AKHTAR N,et al. Corneal nerve loss as a surrogate marker for poor pial collaterals in patients with acute ischemic stroke[J/OL]. Sci Rep,2021,11(1):19718[2024-02-12]. https://doi.org/10.1038/s41598-021-99131-0. [42] LI Y,AN D X,XIE X H,et al. The relationship between neutrophil-to-lymphocyte ratio and cerebral collateral circulation in patients with symptomatic severe intracranial artery stenosis or occlusion[J/OL]. J Clin Neurosci,2023,108:13-18[2024-02-12]. https://doi.org/10.1016/j.jocn.2022.10.022. [43] JI Z X,FANG Q,YU L Q. Collateral circulation and Toll-like receptor 4 levels in patients with acute cerebral infarction after intravenous thrombolysis[J]. Journal of Southern Medical University,2019,39(5):621-626. [44] MECHTOUFF L,BOCHATON T,PACCALET A,et al. Matrix metalloproteinase-9 and monocyte chemoattractant protein-1 are associated with collateral status in acute ischemic stroke with large vessel occlusion[J]. Stroke,2020,51(7):2232-2235. [45] YU F,FENG X J,LI X,et al. Association of plasma metabolic biomarker sphingosine-1-phosphate with cerebral collateral circulation in acute ischemic stroke[J/OL]. Front Physiol,2021,12:720672[2024-02-12]. https://doi.org/10.3389/fphys.2021.720672. [46] MARK I,SEYEDSAADAT S M,BENSON J C,et al. Leukoaraiosis and collateral blood flow in stroke patients with anterior circulation large vessel occlusion[J]. J Neurointerv Surg,2020,12(10):942-945. [47] DONG X F,KONG F Z,SHEN M Q,et al. Triiodothyronine levels were positively correlated with opening of collateral circulation in cerebral infarction patients with large artery atherosclerosis[J]. Arch Med Sci,2019,16(1):51-57. [48] MA J Q,MA Y L,SHUAIB A,et al. Impaired collateral flow in pial arterioles of aged rats during ischemic stroke[J]. Transl Stroke Res,2020,11(2):243-253. [49] FABER J E,ZHANG H,XENAKIS J G,et al. Large differences in collateral blood vessel abundance among individuals arise from multiple genetic variants[J]. J Cereb Blood Flow Metab,2023,43(11):1983-2004. [50] FABER J E,MOORE S M,LUCITTI J L,et al. Sex differences in the cerebral collateral circulation[J]. Transl Stroke Res,2017,8(3):273-283. [51] SCHEIDECKER E,PEREIRA-ZIMMERMANN B,POTRECK A,et al. Role of diabetes in collateral status assessed in CT perfusion-derived dynamic CTA in anterior circulation stroke[J]. Neuroradiology,2022,64(6):1195-1199. [52] SU J H,WOLFF L,VAN DOORMAAL P J,et al. Time dependency of automated collateral scores in computed tomography angiography and computed tomography perfusion images in patients with intracranial arterial occlusion[J]. Neuroradiology,2023,65(2):313-322. [53] WIEGERS E J A,MULDER M J H L,JANSEN I G H,et al. Clinical and imaging determinants of collateral status in patients with acute ischemic stroke in MR CLEAN trial and registry[J]. Stroke,2020,51(5):1493-1502. [54] YI J S,KI H J,JEON Y S,et al. The collateral map:prediction of lesion growth and penumbra after acute anterior circulation ischemic stroke[J]. Eur Radiol,2024,34(3):1411-1421. [55] WOLFF L,SU J H,VAN LOON D,et al. Inter-rater reliability for assessing intracranial collaterals in patients with acute ischemic stroke:comparing 29 raters and an artificial intelligence-based software[J]. Neuroradiology,2022,64(12):2277-2284. [56] WOLFF L,UNIKEN VENEMA S M,LUIJTEN S P R,et al. Diagnostic performance of an algorithm for automated collateral scoring on computed tomography angiography[J]. Eur Radiol,2022,32(8):5711-5718. [57] RAVA R A,SEYMOUR S E,SNYDER K V,et al. Automated collateral flow assessment in patients with acute ischemic stroke using computed tomography with artificial intelligence algorithms[J/OL]. World Neurosurg,2021,155:e748-e760[2024-02-12]. https://doi.org/10.1016/j.wneu.2021.08.136. [58] TAN D,LIU J Y,CHEN S X,et al. Automatic evaluating of multi-phase cranial CTA collateral circulation based on feature fusion attention network model[J]. IEEE Trans Nanobioscience,2023,22(4):789-799. [59] POTRECK A,SCHEIDECKER E,WEYLAND C S,et al. RAPID CT perfusion-based relative CBF identifies good collateral status better than hypoperfusion intensity ratio,CBV-index,and time-to-maximum in anterior circulation stroke[J]. AJNR Am J Neuroradiol,2022,43(7):960-965. [60] GUENEGO A,FAHED R,ALBERS G W,et al. Hypoperfusion intensity ratio correlates with angiographic collaterals in acute ischaemic stroke with M1 occlusion[J]. Eur J Neurol,2020,27(5):864-870. [61] PISANI L,HAUSSEN D C,MOHAMMADEN M,et al. Comparison of CT perfusion software packages for thrombectomy eligibility[J]. Ann Neurol,2023,94(5):848-855. [62] ZHU J Y,MA M M,FANG J H,et al. Prestroke statin use enhances collateralization in acute ischemic stroke patients[J]. Restor Neurol Neurosci,2020,38(4):311-321. |
| [1] | HE Dandan, LI Jian, WANG Chunjuan, LI Shuya. Challenges and Breakthroughs in Basic and Clinical Research of Brain Cytoprotective Agents for Acute Ischemic Stroke in China [J]. Chinese Journal of Stroke, 2026, 21(5): 517-524. |
| [2] | CHENG Xiyue, ZHAO Jingyan, WANG Chunjuan. Research Progress of Edaravone Dexborneol in Brain Cytoprotection for Acute Ischemic Stroke [J]. Chinese Journal of Stroke, 2026, 21(5): 526-532. |
| [3] | YANG Qianqian, ZHANG Meiyang, LU Yao, ZHOU Dongyang, WANG Zhengyilei, Shan Shuyi, LIU Chenhui, WANG Yilong, GUAN Ling. Research Progress on the Anti-Neuroinflammatory Effects and Brain Cytoprotection of Minocycline in Acute Ischemic Stroke: From Mechanisms to Clinical Evidence [J]. Chinese Journal of Stroke, 2026, 21(5): 533-542. |
| [4] | HE Dandan, LI Shuya. Research Progress of PSD-95-Targeted Brain Cytoprotective Agents in Acute Ischemic Stroke Based on STAIR Principles [J]. Chinese Journal of Stroke, 2026, 21(5): 543-552. |
| [5] | CHANG-CAO Wenjing, XU Shuhong, LI Jian, LI Shuya. Research Progress on the Relationship between the Apolipoprotein E Gene and Brain Injury after Ischemic Stroke [J]. Chinese Journal of Stroke, 2026, 21(5): 570-576. |
| [6] | LI Wenyi, JIANG Jiwei, REN Qiwei, WANG Linlin, ZHAO Min, XU Jun. A Study on the Correlation between Apolipoprotein E Gene Polymorphism and Cognitive Function Changes after Stroke [J]. Chinese Journal of Stroke, 2026, 21(5): 577-584. |
| [7] | LIU Yuanhao, WU Lei, YANG Huan, ZHU Jiaying, LI Yazhe. Efficacy and Safety of Different Thrombectomy Devices in the Treatment of Acute Ischemic Stroke: A Retrospective Comparative Study [J]. Chinese Journal of Stroke, 2026, 21(4): 463-470. |
| [8] | OU Ru, LIU Yimin, XU Zhijian, HUANG Wenchun. Dynamic Effects of Lacunes of Presumed Vascular Origin on Health Status in Patients with Acute Ischemic Stroke [J]. Chinese Journal of Stroke, 2026, 21(3): 312-319. |
| [9] | LI Li, DUAN Zhenhui, GAO Aihua, PAN Songbin. Correlation Analysis and Prediction Model Construction of Frailty Index, Nutritional Risk, and Nosocomial Infection Risk after Intravenous Thrombolysis in Elderly Patients with Acute Ischemic Stroke [J]. Chinese Journal of Stroke, 2026, 21(3): 331-337. |
| [10] | National Center for Healthcare Quality Management in Neurological Diseases, Medical Quality Management and Promotion Branch of the Chinese Stroke Association, Interventional Neuroradiology Branch of the Chinese Stroke Association. Expert Recommendations on Evaluation and Improvement of Healthcare Quality for Reperfusion Therapy in Acute Ischemic Stroke (2026) [J]. Chinese Journal of Stroke, 2026, 21(3): 338-352. |
| [11] | ZHANG Zili, ZHAO Ying, MENG Heng, XU Anding. Research Progress on Predicting Futile Recanalization following Endovascular Treatment in Acute Ischemic Stroke [J]. Chinese Journal of Stroke, 2026, 21(3): 378-386. |
| [12] | LIU Mingyue, JIN Shasha, WANG Zhiyong, FU Yanxin, ZHANG Yiwei, NI Jun, WU Liang. Respiratory Rehabilitation Strategies for Severe Stroke: A Review from Evidence-Based Practice to Precision Rehabilitation [J]. Chinese Journal of Stroke, 2026, 21(2): 154-161. |
| [13] | YAO Li, WU Chuanjie. Interpretation of the Key Updates on Endovascular Therapy in the 2026 Guideline for the Early Management of Patients with Acute Ischemic Stroke: A Guideline from the American Heart Association/American Stroke Association [J]. Chinese Journal of Stroke, 2026, 21(2): 234-239. |
| [14] | XIONG Yunyun, LU Zhengzhao, MA Ying, SHAN Dawei, WU Na, HAO Manjun, MA Yujie, WU Shuangzhe, LI Zhixin, SHEN Kejia, TANG Yizhe, WANG Yongjun. Highlights in Stroke in 2025 [J]. Chinese Journal of Stroke, 2026, 21(1): 1-23. |
| [15] | HE Dandan, XU Shuhong, LI Shuya. Clinical Research and Prospects of Novel Intravenous Thrombolytic Agents for Acute Ischemic Stroke within the Standard Time Window [J]. Chinese Journal of Stroke, 2026, 21(1): 24-29. |
| Viewed | ||||||
|
Full text |
|
|||||
|
Abstract |
|
|||||