Clinical significance of cerebral collateral circulation assessment based on Balloon Test Occlusion

doi:10.3969/j.issn.1672-6731.2022.05.003

Abstract

Abstract: Objective To analyze compensatory ability of the cerebral collateral circulation and relevant factors affecting cerebral ischemic tolerance for internal carotid artery (ICA) occlusion by Balloon Test Occlusion (BTO), providing reference basis for the selection of treatment methods in tumors or complicated aneurysms with ICA involved. Methods The clinical data of 87 cases BTO (85 patients, two of whom underwent bilateral BTO) of ICA in Tianjin Huanhu Hospital from June 2016 to September 2021 were analyzed retrospectively. The integrity of anterior or posterior of circulation structure, collateral compensatory capacity, tolerance to ICA occlusion and its influencing factors were analyzed. Results There were 8[9.20% (8/87)] BTO positive cases. The positive rate was of cases with incomplete anterior communicating artery was higher than those with complete anterior communicating artery[3/5 vs. 6.10% (5/82); Fisher's exact probability:P=0.005]. The positive rate of cases with complete fetal posterior cerebral artery (fPCA) which was higher than those without complete fPCA[3/7 vs. 6.25% (5/80); Fisher's exact probability:P=0.015]. The positive rate of cases with non-open anterior circulation which was higher than those cases with open anterior circulation[3/6 vs. 6.17% (5/81); Fisher's exact probability:P=0.009]. The positive rate of cases with non-open posterior circulation which was higher than those cases with open posterior circulation[20% (5/25) vs. 0 (0/59); Fisher's exact probability:P=0.002]. Only the positive rate of patients with anterior circulation opening was higher than that of patients with open anterior circulation and open posterior circulation[13.04% (3/23) vs. 0 (0/3); Fisher's exact probability:P=0.022], neither anterior nor posterior circulation opening were significantly higher than those with only anterior circulation opening[2/2 vs. 13.04% (3/23); Fisher's exact probability:P=0.033] and both anterior and posterior circulation opening[2/2 vs. 0 (0/56); Fisher's exact probability:P=0.001]. Once the ICA occluded, the anterior circulation, the posterior circulation, both of anterior and posterior circulation could provide anterior cerebral artery (ACA) supplied area with compensatory blood flow for 88.10% (74/84), 3.57% (3/84), 5.95% (5/84) cases, respectively. The anterior circulation, the posterior circulation, both anterior and posterior circulation could provide middle cerebral artery (MCA) supplied area with compensatory blood flow for 27.38% (23/84), 16.67% (14/84), 53.57% (45/84) cases, respectively. There were statistically significant differences in the compensatory capacity between ACA (χ²=53.000, P=0.000) and MCA (χ²=54.244, P=0.000). The combined compensatory capacity of both anterior and posterior circulation was higher than that of single anterior circulation (Z=6.754, P=0.000; Z=6.180, P=0.000), single posterior circulation (Z=2.277, P=0.023; Z=5.065, P=0.000) and neither anterior nor posterior circulation (Z=1.991, P=0.047; Z=2.478, P=0.013). Conclusions The anterior circle is functionally much more important than the posterior circle. Non-open anterior circulation, especial absence of anterior communicating artery, complete fPCA, neither anterior nor posterior circulation were highly predictive for intolerance to ICA occlusion. For these cases, attention should be paid to the protection of ICA or active blood flow reconstruction technology to reduce the occurrence of cerebral ischemia. Those cases with both opened anterior circulation and opened posterior circulation provided higher compensatory ability than those with single circulation. For those cases, the ICA of could be sacrificed.

Key words: Arterial occlusive diseases, Carotid artery, internal, Balloon occlusion, Circle of Willis, Collateral circulation

摘要： 目的通过颈内动脉球囊闭塞试验（BTO）评估Willis环前循环和后循环侧支开放情况和代偿能力，以及患者对颈内动脉闭塞耐受能力。方法纳入2016年6月至2021年9月在天津市环湖医院行颈内动脉BTO试验的85例（87侧）患者，BTO试验联合DSA观察前循环和后循环结构完整性、开放比例和代偿能力，对比分析不同组别BTO试验阳性率。结果本组有8侧占9.20%（8/87）BTO试验阳性，前交通动脉缺如、闭塞侧完全胚胎型大脑后动脉、闭塞侧前后循环均不开放患者阳性率分别高于前交通动脉未缺如［3/5对6.10%（5/82）；Fisher确切概率法：P=0.005］、非完全胚胎型大脑后动脉［3/7对6.25%（5/80）；Fisher确切概率法：P=0.015］、前循环开放［3/6对6.17%（5/81）；Fisher确切概率法：P=0.009］和后循环开放［20%（5/25）对0（0/59）；Fisher确切概率法：P=0.002］患者；仅前循环开放患者阳性率高于前后循环均开放患者［13.04%（3/23）对0（0/3）；Fisher确切概率法：P=0.022］，前后循环均不开放患者亦高于仅前循环开放患者［2/2对13.04%（3/23）；Fisher确切概率法：P=0.033］和前后循环均开放患者［2/2对0（0/56）；Fisher确切概率法：P=0.001］。颈内动脉闭塞后，闭塞侧大脑前动脉供血区经单一前循环代偿74侧占88.10%（74/84）、经单一后循环代偿3侧占3.57%（3/84）、经前后循环共同代偿5侧占5.95%（5/84）且均为有效代偿［美国介入和治疗性神经放射学学会/美国介入放射学学会（ASITN/SIR）分级3~4级］，前后循环均未代偿2侧占2.38%（2/84，ASITN/SIR分级为零）；闭塞侧大脑中动脉供血区经单一前循环代偿23侧占27.38%（23/84）且有效代偿为22.62%（19/84），经单一后循环代偿14侧占16.67%（14/84）、经前后循环共同代偿45侧占53.57%（45/84）且均为有效代偿，前后循环均未代偿2侧占2.38%（2/84，ASITN/SIR分级为零）；4种代偿方式对大脑前动脉（χ²=53.000，P=0.000）和大脑中动脉（χ²=54.244，P=0.000）供血区的代偿能力差异有统计学意义，前后循环共同代偿能力高于单一前循环代偿（Z=6.754，P=0.000；Z=6.180，P=0.000）、单一后循环代偿（Z=2.277，P=0.023；Z=5.065，P=0.000）和前后循环均未代偿（Z=1.991，P=0.047；Z=2.478，P=0.013）。结论大脑前循环开放比例较高且代偿能力较强，而前循环不开放尤其是前交通动脉缺如、闭塞侧完全胚胎型大脑后动脉、闭塞侧前后循环均不开放的患者无法耐受颈内动脉闭塞的风险，术中应注意保护颈内动脉。前后循环共同代偿能力高于单一前循环或后循环代偿，闭塞颈内动脉相对安全。

关键词: 动脉闭塞性疾病, 颈内动脉, 气囊阻塞, 大脑动脉环, 侧支循环

SUN Zeng-feng, SHANG Yan-guo, SHENG Zhi-guo, ZHU Hua-yu, TONG Xiao-guang. Clinical significance of cerebral collateral circulation assessment based on Balloon Test Occlusion[J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2022, 22(5): 341-347.

孙增峰, 尚彦国, 盛志国, 朱华雨, 佟小光. 基于球囊闭塞试验的脑血管侧支循环代偿能力评估及临床意义[J]. 中国现代神经疾病杂志, 2022, 22(5): 341-347.

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References

[1] Tong XG, Wang X. Cerebral revascularization for anterior cerebral artery applied in surgery of the complex anterior communicating artery aneurysms[J]. Zhongguo Xian Dai Shen Jing Ji Bing Za Zhi, 2021, 21:527-531.[佟小光, 王轩. 大脑前动脉搭桥术在复杂前交通动脉瘤中的应用[J]. 中国现代神经疾病杂志, 2021, 21:527-531.]
[2] Sun ZF, Shi MG, Shang YG, Tong XG. Application analysis of cerebral revascularization in the treatment of skull base tumors involving internal carotid artery[J]. Zhonghua Shen Jing Wai Ke Za Zhi, 2021, 37:1108-1113.[孙增峰, 施铭岗, 尚彦国, 佟小光. 血流重建在累及颈内动脉的颅底肿瘤治疗中的应用分析[J]. 中华神经外科杂志, 2021, 37:1108-1113.]
[3] Serbinenko FA. Balloon catheterization and occlusion of major cerebral vessels:1994[J]. J Neurosurg, 2007, 107:684-705.
[4] Sun Y, Wang BL, Li Q, Tong XG. Clinical analysis of low flow bypass in the treatment of chronic symptomatic middle cerebral artery occlusion[J]. Zhongguo Xian Dai Shen Jing Ji Bing Za Zhi, 2021, 21:547-552.[孙杨, 王本琳, 李琪, 佟小光. 低流量血管搭桥术治疗慢性症状性大脑中动脉闭塞疗效分析[J]. 中国现代神经疾病杂志, 2021, 21:547-552.]
[5] Liebeskind DS. Collateral circulation[J]. Stroke, 2003, 34:2279-2284.
[6] Liebeskind DS, Cotsonis GA, Saver JL, Lynn MJ, Cloft HJ, Chimowitz MI; Warfarin-Aspirin Symptomatic Intracranial Disease (WASID) Investigators. Collateral circulation in symptomatic intracranial atherosclerosis[J]. J Cereb Blood Flow Metab, 2011, 31:1293-1301.
[7] Wang YL, Luo L. Comparative study on the morphology of Willis circle in three imaging methods[J]. Chongqing Yi Xue, 2019, 48:2660-2663.[王云玲, 罗琳. 3种成像方法中Willis环的形态对比研究[J]. 重庆医学, 2019, 48:2660-2663.]
[8] Linskey ME, Jungreis CA, Yonas H, Hirsch WL Jr, Sekhar LN, Horton JA, Janosky JE. Stroke risk after abrupt internal carotid artery sacrifice:accuracy of preoperative assessment with balloon test occlusion and stable xenon-enhanced CT[J]. AJNR Am J Neuroradiol, 1994, 15:829-843.
[9] Shi HZ, Zheng BJ. Bypass for complex anterior circulation aneurysms[J]. Zhongguo Xian Dai Shen Jing Ji Bing Za Zhi, 2021, 21:532-536.[史怀璋, 郑秉杰. 血管搭桥术在复杂前循环动脉瘤中的应用[J]. 中国现代神经疾病杂志, 2021, 21:532-536.]
[10] Tong XG. Therapeutic effectiveness of bypass and trapping treatment for complex intracranial aneurysms[J]. Zhongguo Xian Dai Shen Jing Ji Bing Za Zhi, 2012, 12:26-31.[佟小光. 颅内复杂动脉瘤搭桥孤立术疗效观察[J]. 中国现代神经疾病杂志, 2012, 12:26-31.]
[11] Rhoton AL Jr. The supratentorial arteries[J]. Neurosurgery, 2002, 51(4 Suppl):S53-120.
[12] Liang F, Fukasaku K, Liu H, Takagi S. A computational model study of the influence of the anatomy of the circle of willis on cerebral hyperperfusion following carotid artery surgery[J]. Biomed Eng Online, 2011, 10:84.
[13] Moore S, David T. A model of autoregulated blood flow in the cerebral vasculature[J]. Proc Inst Mech Eng H, 2008, 222:513-530.
[14] Shatri J, Bexheti S, Shatri M, Kabashi A, Mucaj S. Anatomical variations in the circulus arteriosus cerebri with clinical importance:results of an magnetic resonance angiography study and review of literature[J]. J Clin Imaging Sci, 2021, 11:8.
[15] van Ooij P, Zwanenburg JJ, Visser F, Majoie CB, vanBavel E, Hendrikse J, Nederveen AJ. Quantification and visualization of flow in the Circle of Willis:time-resolved three-dimensional phase contrast MRI at 7 T compared with 3 T[J]. Magn Reson Med, 2013, 69:868-876.
[16] Li Q, Li J, Lv F, Li K, Luo T, Xie P. A multidetector CT angiography study of variations in the circle of Willis in a Chinese population[J]. J Clin Neurosci, 2011, 18:379-383.
[17] Michel E, Liu H, Remley KB, Martin AJ, Madison MT, Kucharczyk J, Truwit CL. Perfusion MR neuroimaging in patients undergoing balloon test occlusion of the internal carotid artery[J]. AJNR Am J Neuroradiol, 2001, 22:1590-1596.
[18] Moore O, Baker HW. Carotid-artery ligation in surgery of the head and neck[J]. Cancer, 1955, 8:712-726.
[19] Norlen G, Falconer M, Jefferson G, Johnson R. The pathology, diagnosis and treatment of intracranial saccular aneurysms[J]. Proc R Soc Med, 1952, 45:291-302.
[20] Nishijima Y, Akamatsu Y, Weinstein PR, Liu J. Collaterals:implications in cerebral ischemic diseases and therapeutic interventions[J]. Brain Res, 2015, 1623:18-29.
[21] Morinaga Y, Nii K, Sakamoto K, Inoue R, Mitsutake T, Hanada H. Presence of an anterior communicating artery as a prognostic factor in revascularization for anterior circulation acute ischemic stroke[J]. World Neurosurg, 2019, 128:e660-663.
[22] Li SX, Chen JH, Zhang YT, Zou ZM, Li YB, Liu SW, Cai J, Chen RC, Bai XX. Role of balloon occlusion test in the treatment of permanent internal carotid artery occlusion[J]. Ju Jie Shou Shu Xue Za Zhi, 2016, 25:603-605.[黎劭学, 陈锦华,张燕婷, 邹志敏, 李颖彬, 刘诗万, 蔡军, 陈锐聪, 白小欣. 球囊闭塞试验在颈内动脉永久闭塞术决策中的参考作用[J]. 局解手术学杂志, 2016, 25:603-605.]
[23] Yang R, Wu H, Chen B, Sun W, Hu X, Wang T, Guo Y, Qiu Y, Dai J. Balloon test occlusion of internal carotid artery in recurrent nasopharyngeal carcinoma before endoscopic nasopharyngectomy:a single center experience[J]. Front Oncol, 2021, 11:674889.
[24] Simonato D, Gargalas S, Cox PJ, Young V, Corkill R, Kuker W, Fuschi M, Houdart E, Labeyrie MA. Aneurysms of the communicating segment of the internal carotid artery with posterior communicating artery agenesis are associated with perforator infarction after embolization[J]. J Neurointerv Surg, 2021, 13:347-352.
[25] Chuang YM, Liu CY, Pan PJ, Lin CP. Posterior communicating artery hypoplasia as a risk factor for acute ischemic stroke in the absence of carotid artery occlusion[J]. J Clin Neurosci, 2008, 15:1376-1381.
[26] Friedrich B, Kempf F, Boeckh-Behrens T, Fischer J, Lehm M, Bernd M, Wunderlich S, Mönch S, Zimmer C, Maegerlein C. Presence of the posterior communicating artery contributes to the clinical outcome after endovascular treatment of patients with MCA occlusions[J]. Cardiovasc Intervent Radiol, 2018, 41:1917-1924.

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