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临床研究
双参数动脉自旋标记成像在评估急性缺血性卒中侧支循环和预后中的应用价值
姜海龙 苏文 陈慧铀 陈宇辰 陈国中 殷信道

Cite this article as: JIANG H L, SU W, CHEN H Y, et al. Application value of arterial spin labeling imaging with dual parameters in evaluating collateral circulation and prognosis of acute ischemic stroke[J]. Chin J Magn Reson Imaging, 2023, 14(3): 53-57, 80.本文引用格式:姜海龙, 苏文, 陈慧铀, 等. 双参数动脉自旋标记成像在评估急性缺血性卒中侧支循环和预后中的应用价值[J]. 磁共振成像, 2023, 14(3): 53-57, 80. DOI:10.12015/issn.1674-8034.2023.03.010.


[摘要] 目的 探讨双参数动脉自旋标记(arterial spin labeling imaging, ASL)成像对急性缺血性卒中(acute ischemic stroke, AIS)侧支循环和预后评估的应用价值。材料与方法 回顾性分析2020年6月至2021年7月南京市第一医院神经内科收治的35例AIS患者的多模态MRI和数字减影血管造影(digital subtraction angiography, DSA)数据。根据梗死灶在双反转时间(inversion time, TI)(1500 ms、2510 ms)的ASL灌注情况,将AIS患者分为3组:早期高灌注组(G1,n=8)、晚期高灌注组(G2,n=6)及非高灌注组(G3,n=21)。采用美国介入和治疗神经放射学学会/介入放射学学会(American Society of Interventional and Therapeutic Neuroradiology/Society of Interventional Radiology, ASITN/SIR)侧支循环评价系统对侧支循环状态进行评估(侧支循环良好:3~4级;侧支循环不良:0~2级),采用改良Rankin量表(modified Rankin scale, mRS)对出院后3个月预后进行评估(预后良好:≤2分;预后不良:>2分)。最后,应用统计学方法分析3组患者侧支循环差异及预后情况。结果 与G3组相比,G1和G2组的入院美国国立卫生研究院卒中量表(National Institutes of Health Stroke Scale, NIHSS)评分较低(G1:2.38±1.69;G2:7.33±1.37;G3:14.81±4.86)、侧支循环良好比例较高(G1:100.00%;G2:83.33%;G3:38.10%)、预后良好比例较高(G1:100.00%;G2:50.00%;G3:42.86%)。G1组和G2组两组侧支循环良好比例无明显差异(100.00% vs. 83.33%;P=0.180),但G1组预后良好率明显高于G2组(100.00% vs. 50.00%;P=0.013)。Spearman相关分析显示G1、G2、G3三组与侧支循环分级呈正相关(r=0.720;P<0.001),与预后mRS评分呈负相关(r=-0.843;P<0.001)。结论 双TI的ASL成像能有效评估AIS患者侧支循环状况和预后情况,为临床制订治疗决策提供了重要依据。
[Abstract] Objective To explore the value of arterial spin labeling (ASL) imaging with dual parameters in evaluating the collateral circulation and prognosis for patients with acute ischemic stroke (AIS).Materials and Methods From June 2022 to July 2022, multi-modal MRI and digital subtraction angiography (DSA) data of 35 AIS patients from Nanjing First Hospital were retrospectively analyzed. All patients were divided into three groups: high perfusion at early stage group (G1, n=21), high perfusion at later stage group (G2, n=8) and no- high perfusion group (G3, n=6) based on the ASL [inversion time (TI)=1500 ms, 2510 ms] imaging features of the infarct lesions. Collateral circulation was divided into good collateral circulation (grade 3-4) and poor collateral circulation (grade 0-2) according to the American Society of Interventional and Therapeutic Neuroradiology/Society of Interventional Radiology (ASITN/SIR). The prognosis was divided into good outcome (≤2 points) and poor outcome (>2 points) according to modified Rankin Scale (mRS) at 3-month follow-up. The differences of collateral circulation and prognosis among three groups were analyzed using statistical methods.Results Compared with G3, G1 and G2 had lower National Institutes of Health Stroke Scale (NIHSS) score, better collateral circulation and good outcome. There was no significant difference in the collateral circulation between G1 and G2 (100.00% vs. 83.33%; P=0.180), while the rate of good outcome in G1 was significantly higher than that in G2 (100.00% vs. 50.00%; P=0.013). Spearman correlation analysis showed that G1, G2, G3 were positively correlated with collateral circulation grade (r=0.720; P<0.001), and negatively correlated with prognosis mRS score (r=-0.843; P<0.001).Conclusions ASL imaging with double inversion time could effectively evaluate the collateral circulation and prognosis of AIS patients, and provide vital evidence for therapeutic decision-making.
[关键词] 急性缺血性卒中;双参数;动脉自旋标记;磁共振成像;侧支循环;预后
[Keywords] acute ischemic stroke;dual parameters;arterial spin labeling;magnetic resonance imaging;collateral circulation;prognosis

姜海龙    苏文    陈慧铀    陈宇辰    陈国中    殷信道 *  

南京医科大学附属南京医院(南京市第一医院)医学影像科,南京 210006

通信作者:殷信道,E-mail:y.163yy@163.com

作者贡献声明:殷信道设计本研究的方案,对稿件重要的智力内容进行了修改;姜海龙起草和撰写稿件,获取、分析或解释本研究的数据;苏文、陈慧铀、陈宇辰、陈国中获取、分析或解释本研究的数据,对稿件重要的智力内容进行了修改;陈国中获得了国家自然科学基金的资助,殷信道获得了江苏省自然科学基金的资助;全体作者都同意发表最后的修改稿,同意对本研究的所有方面负责,确保本研究的准确性和诚信。


基金项目: 国家自然科学基金 82001811 江苏省自然科学基金 BK20201118
收稿日期:2022-11-14
接受日期:2023-03-06
中图分类号:R445.2  R743.3 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2023.03.010
本文引用格式:姜海龙, 苏文, 陈慧铀, 等. 双参数动脉自旋标记成像在评估急性缺血性卒中侧支循环和预后中的应用价值[J]. 磁共振成像, 2023, 14(3): 53-57, 80. DOI:10.12015/issn.1674-8034.2023.03.010.

0 前言

       急性缺血性脑卒中(acute ischemic stroke, AIS)是脑卒中最常见的一类,AIS发病率、致残率和死亡率均较高[1, 2, 3],AIS已经成为危害人类健康的严重疾病[4, 5]。精准评估AIS患者脑血流灌注状况,进而进行针对性治疗,是降低致残率和死亡率的关键[6, 7, 8]。三维动脉自旋标记(3D-arterial spin labeling, 3D-ASL)灌注成像不需要外源性的对比剂,便可对脑血流灌注情况进行无创、定量评估,其测出的脑血流量(cerebral blood flow, CBF)值在可重复性方面表现较好[9, 10, 11]。但3D-ASL中的反转时间(inversion time, TI)这一采集参数会严重影响成像效果,目前国内外联合使用2种不同的TI评估AIS后灌注情况与神经功能受损、预后和侧支循环的关系研究相对较少。本研究采用双TI的ASL成像评估AIS患者灌注状况与侧支循环、预后的关系, 旨在为AIS临床个性化治疗方案的制订提供重要依据。

1 材料与方法

1.1 研究对象

       回顾性分析2020年6月至2021年7月南京市第一医院神经内科收治的35例AIS患者的多模态MRI和数字减影血管造影(digital subtraction angiography, DSA)数据,所有患者均在首次症状发作后24 h内行MRI、DSA检查。其中男18例,女17例,年龄25~80(64.66±13.00)岁。临床主要症状为口齿不清、肢体乏力、活动受限、口角歪斜等。入组标准:(1)符合中国急性缺血性脑卒中诊治指南2018[12]的诊断标准;(2)年龄范围在18~80周岁,既往未有脑卒中病史;(3)弥散加权成像(diffusion weighted imaging, DWI)图像显示急性梗死灶位于单独一侧脑组织;(4)行DSA造影检查。排除标准:(1)合并颅内出血、占位、颅内感染、变性病及其他脑梗死之外的疾病;(2)发病时间不明确的AIS患者。本研究遵守《赫尔辛基宣言》,经南京市第一医院伦理委员会批准,免除受试者知情同意,批准文号:2019-664。

       收集进入组内研究患者的诊疗资料,包括性别、年龄及入院评分,以及既往有关病史如高血压、糖尿病、高脂血症及房颤等,运用改良Rankin量表(modified Rankin Scale, mRS)在出院后3个月进行评分,对其预后的状况进行评估,其中,mRS≤2分为预后良好;mRS>2分为预后差[13, 14]

1.2 图像采集

       采用Siemens Prisma 3.0 T MRI扫描仪、64通道头颈联合线圈。ASL采用三维梯度自旋回波(three dimensional gradient spin echo, 3D GRASE)序列,TI1 1500 ms,TI2 2510 ms,FOV 220 mm×220 mm,TR 4000 ms,TE 16.86 ms,层厚3 mm;DWI采用读出方向分段采样平面回波(readout segmentation of long variabl echo-trains, RESOLVE)序列,采用2个b值(0 s/mm2和1000 s/mm2),FOV 220 mm×220 mm,TR 2400 ms,TE1 54 ms,TE2 89 ms,层厚6 mm;将ASL相关图像采用ASLtbx进行图像后处理[15, 16, 17],分别获得TI为1500 ms、2510 ms的ASL伪彩图,并由2位主治以上职称医师进行评估,若有异议,经协商直至结果一致。

       所有患者血管造影检查均在Siemens DSA数字减影机上进行,通过股动脉穿刺置管后分别对头臂干、左侧颈总动脉和左侧锁骨下动脉进行造影,必要时加做旋转来确保得到有效的头颈动脉正位、斜位和侧位的图像。

1.3 图像分析

       选取DWI图像上急性梗死灶最大的一层,依据此层面伪彩图状况勾画感兴趣区(region of interest, ROI),并分别2次测量每个ROI和镜像区的CBF值,计算相对CBF(relative CBF, rCBF)=患侧CBF平均值/对侧CBF平均值[18, 19]。根据TI分别为1500 ms、2510 ms时rCBF值的不同,将患者分为3组:(1)早期高灌注组(G1),rCBF在TI为1500 ms和2510 ms时均>110%,如图1;(2)晚期高灌注组(G2),rCBF在TI为1500 ms时≤110%,在TI为2510 ms时>110%,如图2;(3)非高灌注组(G3),rCBF在TI为1500 ms和2510 ms时均≤110%,如图3。

图1  女,72岁,左侧肢体乏力4 h,早期高灌注示例图。1A:DWI示右侧侧脑室旁、基底节区并右侧枕叶急性脑梗。1B:rCBF(TI=1500 ms)图,CBF患侧/CBF健侧=43.24/38.09=1.14;1C:rCBF(TI=2510 ms)图,CBF患侧/CBF健侧=59.23/52.27=1.13。1D:DSA示侧支循环丰富,ASITN/SIR分级为4级。图2 女,71岁,头晕呕吐伴右侧肢体无力5 h余,晚期高灌注示例图。2A:DWI示左侧枕叶急性脑梗;2B:rCBF(TI=1500 ms)图,CBF患侧/CBF健侧=33.13/32.08=1.03;2C:rCBF(TI=2510 ms)图,CBF患侧/CBF健侧=56.45/50.39=1.12;2D:DSA示侧支循环良好,ASITN/SIR分级为3级。图3 男,69岁,意识不清4.5 h余,非高灌注示例图。3A:DWI示右侧额颞顶叶急性梗死灶;3B:rCBF(TI=1500 ms)图,CBF患侧/CBF健侧=23.54/42.16=0.56;3C:rCBF(TI=2510 ms图,CBF患侧/CBF健侧=29.79/50.12=0.59;3D:DSA示侧支循环不良,ASITN/SIR分级为0级。DWI:弥散加权成像;CBF:脑血流量;rCBF:相对脑血流量;DSA:数字减影血管造影;ASITN/SIR:美国介入和治疗神经放射学学会/介入放射学分会。
Fig. 1  Female, 72 years old, left limb weakness for 4 h, hyper perfusion at early stage example. 1A: DWI shows acute cerebral infarction in the right lateral ventricle, basal ganglia and right occipital lobe; 1B: rCBF (TI=1500 ms), the CBF in the lesion/ the contralateral CBF=43.24/38.09=1.14; 1C: rCBF (TI=2510 ms), the CBF in the lesion/the contralateral CBF=59.23/52.27=1.13; 1D: DSA shows abundant collateral circulation, and ASITN/SIR is grade 4.
Fig. 2  Female, 71 years old, dizziness and vomiting with right limb weakness for more than 5 h, hyper perfusion at later stage example. 2A: DWI shows acute cerebral infarction in the left occipital lobe; 2B: rCBF (TI=1500 ms), the CBF in the lesion/the contralateral CBF=33.13/32.08=1.03; 2C: rCBF (TI=2510 ms), the CBF in the lesion /the contralateral CBF=56.45/50.39=1.12; 2D: DSA shows good collateral circulation, and ASITN/SIR is grade 3.
Fig. 3  Male, 69 years old, unconsciousness for more than 4.5 years, non-hyperperfusion example. 3A: DWI shows acute infarction in the right frontotemporal parietal lobe; 3B: rCBF (TI=1500 ms), the CBF in the lesion/the contralateral CBF=23.54/42.16=0.56; 3C: rCBF (TI=2510 ms), the CBF in the lesion/the contralateral CBF= 29.79/50.12=0.59; 3D: DSA shows poor collateral circulation, and ASITN/SIR is grade 0. DWI: diffusion-weighted imaging; CBF: cerebral blood flow; rCBF: relative cerebral blood flow; DSA: digital subtraction angiography; ASITN/SIR: American Society of Interventional and Therapeutic Neuroradiology/Society of Interventional Radiology.

1.4 侧支循环评估

       入组患者均由两名有经验的介入科医师针对患者的DSA图像采用双盲法评估其侧支循环情况。评估标准:根据美国介入和治疗神经放射学学会/介入放射学学会(American Society of Interventional and Therapeutic Neuroradiology/Society of Interventional Radiology, ASITN/SIR)侧支循环评价系统进行评估,0级为缺血区域未见明显侧支循环建立;1级为可见侧支代偿,且能够缓慢到达缺血区域周边;2级为可见侧支代偿,且能够快速到达缺血区域周边及部分缺血区;3级为侧支代偿缓慢补偿到所有缺血区域;4级为侧支代偿迅速且充分地补偿到所有缺血区域。根据侧支循环建立情况分组,侧支循环不良:0~2级表示侧支循环未完全建立;侧支循环良好:3~4级表示侧支循环建立。

1.5 统计学分析

       采用SPSS 24.0统计软件进行分析,符合正态分布的计量资料采用均数±标准差(x¯±s)表示,三组间比较采用单因素方差分析;不符合正态分布的计量资料则采用中位数(四分位数间距)表示,三组间比较采用秩和检验进行分析。计数资料采用例数(百分比)表示,三组间比较采用卡方检验分析。应用Spearman相关分析方法分别分析灌注情况与侧支循环、预后的相关性。P<0.05为差异有统计学意义。

2 结果

2.1 基线资料分析

       共35例患者纳入研究,其中G1组8例,G2组6例,G3组21例。与G3组相比,G1组和G2组的入院NIHSS评分较低(G1:2.38±1.69;G2:7.33±1.37;G3:14.81±4.86)、侧支循环良好比例较高(G1:100.00%;G2:83.33%;G3:38.10%)及预后良好比例较高(G1:100.00%;G2:50.00%;G3:42.86%)。G1组和G2组两组侧支循环良好比例无明显差异(100.00% vs. 83.33%;P=0.180),但G1组预后良好率明显高于G2组(100.00% vs. 50.00%;P=0.013)。三组间性别、年龄、高血压、房颤、糖尿病及高脂血症无明显差异(P>0.05)(表1)。

表1  三组间患者临床资料、侧支循环及预后比较
Tab. 1  Comparison of clinical data, collateral circulation and prognosis among the three groups

2.2 相关性分析

       Spearman相关分析显示G1、G2、G3三组与侧支循环分级呈正相关(r=0.720;P<0.001),与预后mRS评分呈负相关(r=-0.843;P<0.001),见图4

图4  G1、G2、G3三组与侧支循环分级、预后评分相关图。
Fig. 4  Correlation diagram of G1, G2 and G3 groups with collateral circulation grade and prognosis score.

3 讨论

       本研究基于双TI ASL成像评估AIS患者灌注状况与侧支循环、预后的关系,结果显示早期高灌注和晚期高灌注患者侧支循环和预后均优于非高灌注组,早期高灌注组与晚期高灌注组间侧支循环虽无明显差异,但早期高灌注组预后明显优于晚期高灌注组,三组的灌注与侧支循环、预后均具有相关性。本研究首次将高灌注细分为早期高灌注和晚期高灌注,进而评分其与侧支循环、预后的关系,可为临床更准确地预测AIS患者的预后提供帮助。

3.1 AIS侧支循环评估的重要性

       AIS是一种由各种原因导致颅内动脉狭窄或闭塞而引起脑组织梗死,并伴随神经细胞、星形胶质细胞等损伤的一类急性血管事件[20, 21, 22],脑侧支循环是指颅内血管局部产生中重度狭窄甚至闭塞时,为了保证问题血管责任供血区基本的血供而形成的吻合血管。侧支循环循环的优良程度会影响全脑的血流变化,且能预测卒中的功能预后[23, 24, 25, 26]。由此可见,准确判断AIS的侧支循环状况对其后续治疗很关键。

3.2 ASL评估侧支循环的价值

       DSA是当前公认的评估侧支循环的黄金标准,既能显示各个阶段的直接血管影像,还能显示侧支血管分布情况,进而能对颅内血管进行分级[27],但其具有创伤性且价格较贵,应用受到一定限制;CT血管成像(CT angiography, CTA)技术可对颅内一级及二级侧支循环进行良好显示,并且与DSA在解剖学方面有较好的一致性[28],但是CTA存在单时相成像、电离辐射等缺陷;磁敏感动态增强MR灌注(dynamic susceptibility contrast MR perfusion, DSC-MRP)成像可以从功能上对侧支循环状态进行评估,并且较DSA评估系统之间有较好一致性[29, 30, 31],但是需要注射钆剂,存在过敏和对比剂残留风险,不利于重复性研究;作为MRI技术中新兴起一种灌注成像序列,3D-ASL序列通过水分子作为内在示踪剂来实现MR灌注成像。该技术之所以能更好地反映组织水平灌注,在于其内源性示踪剂可随意扩散[10, 11]。其与DSC-MRP具有较好一致性[25, 26, 32]。既往研究[28, 29, 33]显示ASL(TI=1500 ms)对梗死后出现低灌注的情况相对敏感,但是其劣势在于评估核心梗死区及缺血半暗带范围上不够准确,存在过分夸大的情况,故而无法在评价脑血流灌注的真实状态上做到客观有效。有学者认为不同延迟时间可能影响脑区CBF值的测量[34],多参数的ASL影像检查在针对评价梗死后脑血流灌注方面存在优势;还有学者通过ASL原始图像动脉移行征象来判断侧支循环情况[35],客观性方面不足;本研究的ASL成像采用了TI=1500 ms、2510 ms两种参数,并且测量了CBF数值,用量化的评价指标来对患者梗死后脑血流灌注状况进行了客观评价。

3.3 双TI ASL成像评估侧支循环、预后的价值

       本研究中,高灌注组患者出院90天mRS评分明显低于非高灌注组,提示高灌注组患者预后相对较好,在TI=1500 ms出现高灌注与颅内血管自发性再通相关;高灌注组患者和晚期高灌注组患者侧支循环要优于非高灌注组,在TI=2510 ms时出现高灌注提示患者侧支循环状况较好,而晚期高灌注组与非高灌注组预后无明显差异,可能原因是即便有侧支血管供应梗死脑组织,但是侧支血管路径相对较长、管腔较细,代偿能力有限。经相关性分析显示,基于双TI ASL成像的灌注情况与AIS患者的侧支循环、预后均具有较好的相关性。该成像技术对AIS患者的灌注情况进行进一步细分,为临床更好地评估患者预后提供有力依据。

3.4 局限性

       本研究仍存在一定的局限性。首先,本研究样本量纳入较少,后期将会增大样本量以验证结果的可靠性;其次,灌注情况未与血管狭窄程度进行对比;最后,患者的预后受诸多因素影响,未将患者的治疗情况如血管再通情况等纳入研究,后期将进一步增加变量进行分析。

4 结论

       综上所述,基于双TI的ASL成像的灌注情况与AIS患者侧支循环和预后密切相关,可为临床个性化治疗方案的制订提供重要依据。

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