Research progress on collateral circulation scores of CT angiography and prognosis of ischemic stroke_West China Medical Journal

Authors：

LIU Dong ,  LIU Junfeng

Department of Neurology, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P. R. China;

Corresponding author：

LIU Junfeng, Email: junfengliu225@outlook.com

Keywords：

Ischemic stroke; collateral circulation; CT angiography; scoring scale

DOI：

10.7507/1002-0179.202204129

Video：

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Good collateral circulation can effectively improve the prognosis of patients with severe stenosis or occlusion of cerebral blood supply artery. Studies have shown that CT angiography (CTA) can non-invasively and intuitively evaluate the degree of stenosis and collateral blood flow in diseased vessels. Rapid and accurate CTA collateral circulation score is of great significance for clinical decision-making and judging the prognosis of ischemic stroke. At present, there are many scoring scales based on CTA collateral circulation. This article will review the existing 7 CTA collateral circulation scoring scales, the advantages and disadvantages of clinical application and related research progress in predicting prognosis, aiming to provide a reference for clinicians to choose the collateral circulation score scale and the best treatment plan according to different situations.

Citation： LIU Dong, LIU Junfeng. Research progress on collateral circulation scores of CT angiography and prognosis of ischemic stroke. West China Medical Journal, 2022, 37(9): 1388-1394. doi: 10.7507/1002-0179.202204129 Copy

1.	贾建平, 陈生弟. 神经病学. 8 版. 北京: 人民卫生出版社, 2018: 186-242.
2.	中国卒中学会脑血流与代谢分会. 缺血性卒中脑侧支循环评估与干预中国指南(2017). 中华内科杂志, 2017, 56(6): 460-471.
3.	He H, Qian ZM, Sheng Y, et al. Assessment of cerebral collateral flow with single-phase computed tomography angiography-based multimodal scales in patients with acute ischemic stroke. J Comput Assist Tomogr, 2020, 44(5): 708-713.
4.	王国防. 基于 CTA 的侧支循环评分方法比较研究. 苏州: 苏州大学, 2017.
5.	Chatterjee D, Nagarajan K, Narayan SK, et al. Regional leptomeningeal collateral score by computed tomographic angiography correlates with 3-month clinical outcome in acute ischemic stroke. Brain Circ, 2020, 6(2): 107-115.
6.	Baydemir R, Aykaç Ö, Acar BA, et al. Role of modified TAN score in predicting prognosis in patients with acute ischemic stroke undergoing endovascular therapy. Clin Neurol Neurosurg, 2021, 210: 106978.
7.	Shafie M, Yu W. Recanalization therapy for acute ischemic stroke with large vessel occlusion: where we are and what comes next?. Transl Stroke Res, 2021, 12(3): 369-381.
8.	Seker F, Pereira-Zimmermann B, Pfaff J, et al. Collateral scores in acute ischemic stroke: a retrospective study assessing the suitability of collateral scores as standalone predictors of clinical outcome. Clin Neuroradiol, 2020, 30(4): 789-793.
9.	Maas MB, Lev MH, Ay H, et al. Collateral vessels on CT angiography predict outcome in acute ischemic stroke. Stroke, 2009, 40(9): 3001-3005.
10.	张英, 汪桦, 陆丰, 等. 两种 CT 血管造影侧支循环评分对大脑中动脉闭塞性脑卒中患者预后的评价价值研究. 中国全科医学, 2018, 21(24): 2937-2942.
11.	Tan IY, Demchuk AM, Hopyan J, et al. CT angiography clot burden score and collateral score: correlation with clinical and radiologic outcomes in acute middle cerebral artery infarct. AJNR Am J Neuroradiol, 2009, 30(3): 525-531.
12.	余翔, 赵小英, 刘斌. 基于 CTA 不同评分量表评估急性缺血性脑卒中侧支建立的研究进展. 国际医学放射学杂志, 2020, 43(5): 550-554.
13.	Jansen IGH, Berkhemer OA, Yoo AJ, et al. Comparison of CTA- and DSA-based collateral flow assessment in patients with anterior circulation stroke. AJNR Am J Neuroradiol, 2016, 37(11): 2037-2042.
14.	Nordmeyer H, Webering N, Chapot R, et al. The association between collateral status, recanalization and long term outcome in stroke patients treated with stent retrievers - are there indications not to perform thrombectomy based on CT angiography?. J Neuroradiol, 2017, 44(3): 217-222.
15.	Menon BK, Smith EE, Modi J, et al. Regional leptomeningeal score on CT angiography predicts clinical and imaging outcomes in patients with acute anterior circulation occlusions. AJNR Am J Neuroradiol, 2011, 32(9): 1640-1645.
16.	陈艳, 赵佳驹, 吴波. 区域软脑膜侧支循环评分与 Tan 侧支循环评分预测前循环缺血性卒中静脉溶栓预后. 中国现代神经疾病杂志, 2018, 18(9): 678-682.
17.	Liu X, Pu Y, Pan Y, et al. Multi-mode CT in the evaluation of leptomeningeal collateral flow and the related factors: comparing with digital subtraction angiography. Neurol Res, 2016, 38(6): 504-509.
18.	高冬艳. CTA 评估大脑中动脉 M1 段闭塞急性脑梗死病人的侧支循环及其与静脉溶栓预后的关系. 中西医结合心脑血管病杂志, 2017, 15(23): 3063-3066.
19.	Miteff F, Levi CR, Bateman GA, et al. The independent predictive utility of computed tomography angiographic collateral status in acute ischaemic stroke. Brain, 2009, 132(Pt 8): 2231-2238.
20.	Yeo LL, Paliwal P, Teoh HL, et al. Assessment of intracranial collaterals on CT angiography in anterior circulation acute ischemic stroke. AJNR Am J Neuroradiol, 2015, 36(2): 289-294.
21.	Cipolla MJ. Thomas Willis lecture: targeting brain arterioles for acute stroke treatment. Stroke, 2021, 52(7): 2465-2477.
22.	Menon BK, d’Esterre CD, Qazi EM, et al. Multiphase CT angiography: a new tool for the imaging triage of patients with acute ischemic stroke. Radiology, 2015, 275(2): 510-520.
23.	谢健. CTA 侧支循环与急性缺血性卒中患者再灌注治疗预后的相关性研究. 南京: 东南大学, 2019.
24.	Seker F, Potreck A, Möhlenbruch M, et al. Comparison of four different collateral scores in acute ischemic stroke by CT angiography. J Neurointerv Surg, 2016, 8(11): 1116-1118.
25.	张正义, 熊洁, 敬茜, 等. 多时相 CT 血管造影对急性缺血性脑卒中患者侧支循环评估价值及溶栓治疗指导作用. 实用医院临床杂志, 2021, 18(2): 167-170.
26.	Goyal M, Demchuk AM, Menon BK, et al. Randomized assessment of rapid endovascular treatment of ischemic stroke. N Engl J Med, 2015, 372(11): 1019-1030.
27.	Menon BK, O’Brien B, Bivard A, et al. Assessment of leptomeningeal collaterals using dynamic CT angiography in patients with acute ischemic stroke. J Cereb Blood Flow Metab, 2013, 33(3): 365-371.
28.	Menon BK, Qazi E, Nambiar V, et al. Differential effect of baseline computed tomographic angiography collaterals on clinical outcome in patients enrolled in the interventional management of stroke Ⅲ trial. Stroke, 2015, 46(5): 1239-1244.
29.	Vagal A, Menon BK, Foster LD, et al. Association between CT angiogram collaterals and CT perfusion in the interventional management of stroke III trial. Stroke, 2016, 47(2): 535-538.
30.	Lee J, Park DW, Kim YS, et al. Arterial spin labeling signal ratio between the lesion and contralateral sides for evaluation of acute middle cerebral artery infarct. Medicine (Baltimore), 2022, 101(2): e28569.
31.	Cui C, Hong Y, Bao J, et al. The diagnostic reliability and validity of noninvasive imaging modalities to assess leptomeningeal collateral flow for ischemic stroke patients: a systematic review and meta-analysis. Medicine (Baltimore), 2021, 100(18): e25543.
32.	Tian H, Chen C, Garcia-Esperon C, et al. Dynamic CT but not optimized multiphase CT angiography accurately identifies CT perfusion target mismatch ischemic stroke patients. Front Neurol, 2019, 10: 1130.
33.	Weiss D, Kraus B, Rubbert C, et al. Systematic evaluation of computed tomography angiography collateral scores for estimation of long-term outcome after mechanical thrombectomy in acute ischaemic stroke. Neuroradiol J, 2019, 32(4): 277-286.
34.	Bisson DA, Mahmoudian D, Shatil AS, et al. Single-phase CT angiography: collateral grade is independent of scan weighting. Neuroradiology, 2019, 61(1): 19-28.
35.	Park JS, Kwak HS, Chung GH, et al. The prognostic value of CT-angiographic parameters after reperfusion therapy in acute ischemic stroke patients with internal carotid artery terminus occlusion: leptomeningeal collateral status and clot burden score. J Stroke Cerebrovasc Dis, 2018, 27(10): 2797-2803.
36.	Zhang X, Zhang M, Ding W, et al. Distinct predictive role of collateral status on clinical outcome in variant stroke subtypes of acute large arterial occlusion. Eur J Neurol, 2018, 25(2): 293-300.
37.	Zhang S, Chen W, Tang H, et al. The prognostic value of a four-dimensional CT angiography-based collateral grading scale for reperfusion therapy in acute ischemic stroke patients. PLoS One, 2016, 11(8): e0160502.
38.	Choi JY, Kim EJ, Hong JM, et al. Conventional enhancement CT: a valuable tool for evaluating pial collateral flow in acute ischemic stroke. Cerebrovasc Dis, 2011, 31(4): 346-352.
39.	Nigron A, Bourgois N, Dao S, et al. Anterior ischemic stroke: comparison of two clinical outcome prediction scores through the investigation of cerebral collaterals using multiphase CT angiography. J Neuroradiol, 2021, 48(6): 438-445.
40.	Sillanpää N, Saarinen JT, Rusanen H. Computed tomography angiography source images closely reflect the integrity of collateral circulation. J Neuroradiol, 2015, 42(5): 261-268.
41.	van den Wijngaard IR, Boiten J, Holswilder G, et al. Impact of collateral status evaluated by dynamic computed tomographic angiography on clinical outcome in patients with ischemic stroke. Stroke, 2015, 46(12): 3398-3404.
42.	陈伟莉. 动态 CTA 评估急性缺血性脑卒中侧支血流与静脉溶栓预后的关系. 杭州: 浙江大学, 2014.
43.	Cao R, Qi P, Liu Y, et al. Improving prognostic evaluation by 4D CTA for endovascular treatment in acute ischemic stroke patients: a preliminary study. J Stroke Cerebrovasc Dis, 2019, 28(7): 1971-1978.
44.	Ma YC, Chen AQ, 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. Technol Health Care, 2022, 30(4): 967-979.
45.	叶国伟, 许兵, 邹建勋, 等. 多模式 CT 定量评估急性缺血性脑卒中侧支循环及缺血半暗带与预后的应用. 医学影像学杂志, 2020, 30(10): 1757-1760.
46.	王庆松. 动态 CTA 模拟 ASITN/SIR 的侧支评分预测急性缺血性卒中血管内治疗患者的预后. 杭州: 浙江大学, 2017.

1. 贾建平, 陈生弟. 神经病学. 8 版. 北京: 人民卫生出版社, 2018: 186-242.
2. 中国卒中学会脑血流与代谢分会. 缺血性卒中脑侧支循环评估与干预中国指南(2017). 中华内科杂志, 2017, 56(6): 460-471.
3. He H, Qian ZM, Sheng Y, et al. Assessment of cerebral collateral flow with single-phase computed tomography angiography-based multimodal scales in patients with acute ischemic stroke. J Comput Assist Tomogr, 2020, 44(5): 708-713.
4. 王国防. 基于 CTA 的侧支循环评分方法比较研究. 苏州: 苏州大学, 2017.
5. Chatterjee D, Nagarajan K, Narayan SK, et al. Regional leptomeningeal collateral score by computed tomographic angiography correlates with 3-month clinical outcome in acute ischemic stroke. Brain Circ, 2020, 6(2): 107-115.
6. Baydemir R, Aykaç Ö, Acar BA, et al. Role of modified TAN score in predicting prognosis in patients with acute ischemic stroke undergoing endovascular therapy. Clin Neurol Neurosurg, 2021, 210: 106978.
7. Shafie M, Yu W. Recanalization therapy for acute ischemic stroke with large vessel occlusion: where we are and what comes next?. Transl Stroke Res, 2021, 12(3): 369-381.
8. Seker F, Pereira-Zimmermann B, Pfaff J, et al. Collateral scores in acute ischemic stroke: a retrospective study assessing the suitability of collateral scores as standalone predictors of clinical outcome. Clin Neuroradiol, 2020, 30(4): 789-793.
9. Maas MB, Lev MH, Ay H, et al. Collateral vessels on CT angiography predict outcome in acute ischemic stroke. Stroke, 2009, 40(9): 3001-3005.
10. 张英, 汪桦, 陆丰, 等. 两种 CT 血管造影侧支循环评分对大脑中动脉闭塞性脑卒中患者预后的评价价值研究. 中国全科医学, 2018, 21(24): 2937-2942.
11. Tan IY, Demchuk AM, Hopyan J, et al. CT angiography clot burden score and collateral score: correlation with clinical and radiologic outcomes in acute middle cerebral artery infarct. AJNR Am J Neuroradiol, 2009, 30(3): 525-531.
12. 余翔, 赵小英, 刘斌. 基于 CTA 不同评分量表评估急性缺血性脑卒中侧支建立的研究进展. 国际医学放射学杂志, 2020, 43(5): 550-554.
13. Jansen IGH, Berkhemer OA, Yoo AJ, et al. Comparison of CTA- and DSA-based collateral flow assessment in patients with anterior circulation stroke. AJNR Am J Neuroradiol, 2016, 37(11): 2037-2042.
14. Nordmeyer H, Webering N, Chapot R, et al. The association between collateral status, recanalization and long term outcome in stroke patients treated with stent retrievers - are there indications not to perform thrombectomy based on CT angiography?. J Neuroradiol, 2017, 44(3): 217-222.
15. Menon BK, Smith EE, Modi J, et al. Regional leptomeningeal score on CT angiography predicts clinical and imaging outcomes in patients with acute anterior circulation occlusions. AJNR Am J Neuroradiol, 2011, 32(9): 1640-1645.
16. 陈艳, 赵佳驹, 吴波. 区域软脑膜侧支循环评分与 Tan 侧支循环评分预测前循环缺血性卒中静脉溶栓预后. 中国现代神经疾病杂志, 2018, 18(9): 678-682.
17. Liu X, Pu Y, Pan Y, et al. Multi-mode CT in the evaluation of leptomeningeal collateral flow and the related factors: comparing with digital subtraction angiography. Neurol Res, 2016, 38(6): 504-509.
18. 高冬艳. CTA 评估大脑中动脉 M1 段闭塞急性脑梗死病人的侧支循环及其与静脉溶栓预后的关系. 中西医结合心脑血管病杂志, 2017, 15(23): 3063-3066.
19. Miteff F, Levi CR, Bateman GA, et al. The independent predictive utility of computed tomography angiographic collateral status in acute ischaemic stroke. Brain, 2009, 132(Pt 8): 2231-2238.
20. Yeo LL, Paliwal P, Teoh HL, et al. Assessment of intracranial collaterals on CT angiography in anterior circulation acute ischemic stroke. AJNR Am J Neuroradiol, 2015, 36(2): 289-294.
21. Cipolla MJ. Thomas Willis lecture: targeting brain arterioles for acute stroke treatment. Stroke, 2021, 52(7): 2465-2477.
22. Menon BK, d’Esterre CD, Qazi EM, et al. Multiphase CT angiography: a new tool for the imaging triage of patients with acute ischemic stroke. Radiology, 2015, 275(2): 510-520.
23. 谢健. CTA 侧支循环与急性缺血性卒中患者再灌注治疗预后的相关性研究. 南京: 东南大学, 2019.
24. Seker F, Potreck A, Möhlenbruch M, et al. Comparison of four different collateral scores in acute ischemic stroke by CT angiography. J Neurointerv Surg, 2016, 8(11): 1116-1118.
25. 张正义, 熊洁, 敬茜, 等. 多时相 CT 血管造影对急性缺血性脑卒中患者侧支循环评估价值及溶栓治疗指导作用. 实用医院临床杂志, 2021, 18(2): 167-170.
26. Goyal M, Demchuk AM, Menon BK, et al. Randomized assessment of rapid endovascular treatment of ischemic stroke. N Engl J Med, 2015, 372(11): 1019-1030.
27. Menon BK, O’Brien B, Bivard A, et al. Assessment of leptomeningeal collaterals using dynamic CT angiography in patients with acute ischemic stroke. J Cereb Blood Flow Metab, 2013, 33(3): 365-371.
28. Menon BK, Qazi E, Nambiar V, et al. Differential effect of baseline computed tomographic angiography collaterals on clinical outcome in patients enrolled in the interventional management of stroke Ⅲ trial. Stroke, 2015, 46(5): 1239-1244.
29. Vagal A, Menon BK, Foster LD, et al. Association between CT angiogram collaterals and CT perfusion in the interventional management of stroke III trial. Stroke, 2016, 47(2): 535-538.
30. Lee J, Park DW, Kim YS, et al. Arterial spin labeling signal ratio between the lesion and contralateral sides for evaluation of acute middle cerebral artery infarct. Medicine (Baltimore), 2022, 101(2): e28569.
31. Cui C, Hong Y, Bao J, et al. The diagnostic reliability and validity of noninvasive imaging modalities to assess leptomeningeal collateral flow for ischemic stroke patients: a systematic review and meta-analysis. Medicine (Baltimore), 2021, 100(18): e25543.
32. Tian H, Chen C, Garcia-Esperon C, et al. Dynamic CT but not optimized multiphase CT angiography accurately identifies CT perfusion target mismatch ischemic stroke patients. Front Neurol, 2019, 10: 1130.
33. Weiss D, Kraus B, Rubbert C, et al. Systematic evaluation of computed tomography angiography collateral scores for estimation of long-term outcome after mechanical thrombectomy in acute ischaemic stroke. Neuroradiol J, 2019, 32(4): 277-286.
34. Bisson DA, Mahmoudian D, Shatil AS, et al. Single-phase CT angiography: collateral grade is independent of scan weighting. Neuroradiology, 2019, 61(1): 19-28.
35. Park JS, Kwak HS, Chung GH, et al. The prognostic value of CT-angiographic parameters after reperfusion therapy in acute ischemic stroke patients with internal carotid artery terminus occlusion: leptomeningeal collateral status and clot burden score. J Stroke Cerebrovasc Dis, 2018, 27(10): 2797-2803.
36. Zhang X, Zhang M, Ding W, et al. Distinct predictive role of collateral status on clinical outcome in variant stroke subtypes of acute large arterial occlusion. Eur J Neurol, 2018, 25(2): 293-300.
37. Zhang S, Chen W, Tang H, et al. The prognostic value of a four-dimensional CT angiography-based collateral grading scale for reperfusion therapy in acute ischemic stroke patients. PLoS One, 2016, 11(8): e0160502.
38. Choi JY, Kim EJ, Hong JM, et al. Conventional enhancement CT: a valuable tool for evaluating pial collateral flow in acute ischemic stroke. Cerebrovasc Dis, 2011, 31(4): 346-352.
39. Nigron A, Bourgois N, Dao S, et al. Anterior ischemic stroke: comparison of two clinical outcome prediction scores through the investigation of cerebral collaterals using multiphase CT angiography. J Neuroradiol, 2021, 48(6): 438-445.
40. Sillanpää N, Saarinen JT, Rusanen H. Computed tomography angiography source images closely reflect the integrity of collateral circulation. J Neuroradiol, 2015, 42(5): 261-268.
41. van den Wijngaard IR, Boiten J, Holswilder G, et al. Impact of collateral status evaluated by dynamic computed tomographic angiography on clinical outcome in patients with ischemic stroke. Stroke, 2015, 46(12): 3398-3404.
42. 陈伟莉. 动态 CTA 评估急性缺血性脑卒中侧支血流与静脉溶栓预后的关系. 杭州: 浙江大学, 2014.
43. Cao R, Qi P, Liu Y, et al. Improving prognostic evaluation by 4D CTA for endovascular treatment in acute ischemic stroke patients: a preliminary study. J Stroke Cerebrovasc Dis, 2019, 28(7): 1971-1978.
44. Ma YC, Chen AQ, 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. Technol Health Care, 2022, 30(4): 967-979.
45. 叶国伟, 许兵, 邹建勋, 等. 多模式 CT 定量评估急性缺血性脑卒中侧支循环及缺血半暗带与预后的应用. 医学影像学杂志, 2020, 30(10): 1757-1760.
46. 王庆松. 动态 CTA 模拟 ASITN/SIR 的侧支评分预测急性缺血性卒中血管内治疗患者的预后. 杭州: 浙江大学, 2017.

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