TWIST技术在评估急性缺血性卒中侧支循环中的应用价值

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• 临床研究 •

王思雨艾中萍吴倩倩姜海龙姜亮陈国中殷信道

Cite this article as: Wang SY, Ai ZP, Wu QQ, et al. Application value of TWIST technique in evaluating collateral circulation in acute ischemic stroke[J]. Chin J Magn Reson Imaging, 2022, 13(5): 11-16.本文引用格式：王思雨, 艾中萍, 吴倩倩, 等. TWIST技术在评估急性缺血性卒中侧支循环中的应用价值[J]. 磁共振成像, 2022, 13(5): 11-16. DOI:10.12015/issn.1674-8034.2022.05.003.

摘要

[摘要] 目的探讨基于磁共振时间分辨交叉随机轨迹显像(time-resolved angiography with interleaved stochastic trajectories，TWIST)技术在评估急性缺血性卒中侧支循环中的应用价值。材料与方法 回顾性分析2020年8月至2021年8月南京市第一医院神经内科收治的28例急性缺血性卒中患者的一般临床资料及影像资料，所有患者均接受了磁共振TWIST、灌注加权成像和数字减影血管造影(digital subtraction angiography，DSA)检查。DSA和TWIST图像的侧支循环分级分别参考美国介入与治疗神经放射学学会/介入放射学会(American Society of Interventional and Therapeutic Neuroradiology/Society of Interventional Radiology，ASITN/SIR)分级系统和改良的ASITN/SIR评分量表。Kappa系数用于分析侧支循环分级在不同观察者间的一致性。χ²检验用于分析TWIST和DSA图像的侧支循环分级结果的组间差异。根据TWIST图像的侧支循环分级将患者分为侧支循环丰富组和侧支循环不丰富组，ASITN/SIR分级3～4级表示侧支循环丰富，0～2级表示侧支循环不丰富，对比两组患者的临床资料和低灌注强度比值(hypoperfusion intensity ratio，HIR)。采用Spearman秩相关系数分析HIR与TWIST图像的侧支循环分级的相关性。结果 TWIST (Kappa=0.826)和DSA (Kappa=0.856)图像的侧支循环分级在不同观察者间均具有高度一致性。TWIST和DSA图像的侧支循环分级结果组间差异无统计学意义(χ²=0.865，P=0.929)。与侧支循环不丰富组(13例)相比，侧支循环丰富组(15例) HIR更低(0.30±0.08 vs. 0.43±0.06，t=-5.156，P＜0.001)，相关分析显示HIR与TWIST图像的侧支循环分级呈负相关(r=-0.882，P＜0.001)。结论磁共振TWIST技术可无创评估急性缺血性卒中的侧支循环，在侧支循环诊断中具有较高的价值，可应用于临床。

[Abstract] Objective To evaluate the value of time-resolved with interleaved stochastic trajectories (TWIST) technology in the evaluation of collateral circulation in acute ischemic stroke.Materials and Methods The general clinical data of 28 patients with acute ischemic stroke treated in the Department of Neurology of Nanjing First Hospital from August 2020 to August 2021 were analyzed retrospectively. All patients underwent TWIST, perfusion weighted imaging and digital subtraction angiography (DSA). The collateral circulation classification of DSA and TWIST images refer to the classification system of American Society of Interventional and Therapeutic Neuroradiology/Society of Interventional Radiology (ASITN/SIR) and the modified ASITN/SIR score scale, respectively. Kappa coefficient was used to analyze the consistency of collateral circulation classification among different observers. χ² test was used to analyze the inter group differences of collateral circulation classification results of TWIST and DSA images. The patients were divided into abundant collateral circulation group and insufficient collateral circulation group according to the collateral circulation classification of TWIST images, ASITN/SIR score 3-4 indicates abundant collateral circulation and score 0-2 indicates insufficient collateral circulation. The clinical data and hypoperfusion intensity ratio (HIR) of the two groups were compared. Spearman rank correlation coefficient was used to analyze the correlation between HIR and collateral circulation classification of TWIST images.Results The collateral circulation scores of TWIST (Kappa=0.826) and DSA (Kappa=0.856) images were both highly consistent among different observers. There was no significant difference in collateral circulation classification between TWIST and DSA images (χ²=0.865, P=0.929). The HIR in the abundant collateral circulation group (15 cases) was lower than that in the insufficient collateral circulation group (13 cases) (0.30±0.08 vs. 0.43±0.06, t=-5.156, P＜0.001). Correlation analysis showed that HIR was negatively correlated with the classification of collateral circulation in TWIST images (r=-0.882, P＜0.001).Conclusions Magnetic resonance TWIST can noninvasive evaluate collateral circulation of acute ischemic stroke. It has high value in collateral circulation diagnosis and can be used in clinic.

[关键词] 急性缺血性卒中；磁共振成像；时间分辨交叉随机轨迹显像；侧支循环；低灌注强度比值

[Keywords] acute ischemic stroke；magnetic resonance imaging；time-resolved angiography with interleaved stochastic trajectories；collateral circulation；hypoperfusion intensity ratio

作者信息

王思雨 ¹ 艾中萍 ¹ 吴倩倩 ² 姜海龙 ¹ 姜亮 ¹ 陈国中 ¹ 殷信道 ^1*

¹ 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

² 南京医科大学附属南京医院(南京市第一医院)临床医学工程处，南京　210006

殷信道，E-mail：y.163yy@163.com

作者利益冲突声明：全部作者均声明无利益冲突。

出版信息

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：2021-10-27

接受日期：2022-04-29

中图分类号：R445.2 R743.3

文献标识码：A

DOI: 10.12015/issn.1674-8034.2022.05.003

本文引用格式：王思雨, 艾中萍, 吴倩倩, 等. TWIST技术在评估急性缺血性卒中侧支循环中的应用价值[J]. 磁共振成像, 2022, 13(5): 11-16. DOI:10.12015/issn.1674-8034.2022.05.003.

正文

急性缺血性卒中是指由脑组织缺氧坏死继而引起神经系统功能不同程度损伤的一种脑血管病，约占全部卒中的69.6%～70.8%^[¹^,²^]。研究显示，脑侧支循环影响卒中患者缺血半暗带血供、梗死灶体积进展以及卒中复发和出血转化的风险预测^[³^,⁴^]，因此早期快速准确地评估侧支循环对于指导急性缺血性卒中患者临床治疗方案的选择和预后评估至关重要。

目前临床上已有多种影像学检查方法用于评估侧支循环，数字减影血管造影(digital subtraction angiography，DSA)是评估侧支循环的“金标准”^[⁵^]，但检查的适用性受到其侵入性和相关风险的限制^[⁶^]。常规对比增强磁共振血管成像(contrast enhanced magnetic resonance angiography，CE-MRA)可以评估侧支循环^[⁷^,⁸^]，然其存在一些技术上的局限性，比如对比剂峰值通过时间不同步、扫描时间延迟造成的静脉血管污染图像和低时间分辨率等^[⁹^]。近年来，随着磁共振新技术的不断发展，4D磁共振血管成像(magnetic resonance angiography，MRA)在急性缺血性卒中患者的血管评估中受到临床医生的日益关注^[¹⁰^]。

时间分辨交叉随机轨迹显像(time-resolved angiography with interleaved stochastic trajectories，TWIST)技术是西门子系统的一种非侵入性的时间分辨4D MRA技术，它通过运用更为巧妙灵活的K空间采集策略，在牺牲了一点空间分辨率和图像信噪比的前提下，提高时间分辨率以获得动态血流信息^[¹¹^,¹²^,¹³^]。Seeger等^[¹⁴^]研究显示TWIST技术在诊断卒中患者血管狭窄诊断中具有高敏感性和高阴性预测价值。Le Bras等^[¹⁵^]研究显示TWIST技术与DSA在诊断卒中患者血管狭窄位置上没有显著性差异。然而，目前仅有少数文献报道过TWIST技术作为一种有用的卒中侧支成像方法的可能性^[¹⁶^]，且缺乏与标准侧支循环分级的对比。因此，本研究利用TWIST技术提供动态信息，以DSA图像和低灌注强度比值(hypoperfusion intensity ratio，HIR)^[¹⁷^]为参考进行对比研究，旨在探讨磁共振TWIST技术在评估急性缺血性卒中患者侧支循环中的应用价值。

1 资料与方法

1.1 研究对象

回顾性分析2020年8月至2021年8月南京市第一医院神经内科收治的28例急性缺血性卒中患者的一般临床资料[男19例，女9例，年龄50～85 (67.85±8.63)岁]及影像资料。纳入标准：(1) 48 h内行磁共振TWIST、灌注加权成像(perfusion weighted imaging，PWI)和DSA检查；(2)经DSA检查证实至少存在1支颅内动脉中重度狭窄或闭塞；(3) TWIST图像满足诊断要求，图像质量评分≥2分。排除标准：(1) DSA检查前已行脑血管重建手术；(2)并发颅内出血、占位、肿瘤、感染、血管畸形等其他脑梗死之外的疾病；(3)影像质量不合格或一般临床资料不完整。本研究经南京医科大学伦理委员会批准，免除受试者知情同意，批准文号：2019-664。

1.2 MRI扫描方法

所有患者均在西门子医疗系统的(Magnetom Prisma，德国) 3.0 T MRI扫描设备上进行检查，使用8通道头颈专用线圈，扫描序列包括PWI和TWIST序列。具体参数如下：PWI：重复时间(repetition time，TR) 2000 ms，回波时间(echo time，TE) 30 ms，视野(field of view，FOV) 224 mm×224 mm，矩阵96×93，层厚4 mm，翻转角(flip angle，FA) 90°，扫描时间88 s；TWIST：TR 2.72 ms，TE 0.99 ms，FOV 380 mm×332 mm，体素1.1 mm×1.1 mm×1.2 mm，层厚1.2 mm，A区采样密度15%，B区采样密度20%，并行采集技术为GRAPPA，加速因子为6，扫描时间73 s，共采集42期数据(第1期为蒙片期)。

1.3 影像分析

参考图像质量评分标准对TWIST图像进行图像质量评分：1分：图像质量差，有明显的模糊或伪影，无法评价；2分：良好、足够的血管边界，用于诊断的足够图像质量；3分：优秀、清晰定义的血管边界，具有高诊断可信度的图像质量。DSA的侧支循环分级参考美国介入与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)分级系统^[¹⁸^]。将41期TWIST图像大致分为动脉期、静脉期和静脉晚期，TWIST图像的侧支循环分级参考改良的ASITN/SIR评分量表^[¹⁹^]：0分：在任何时相内，在缺血区域内没有或仅有少量软脑膜侧支；1分：直至静脉晚期才可在缺血区域内见到部分侧支循环形成；2分：静脉期以前可见缺血区域内部分侧支循环形成；3分：静脉晚期可见缺血区域内完全的侧支循环形成；4分：在静脉期以前可见完全的侧支循环形成。根据TWIST图像的侧支循环分级将患者分为侧支循环丰富组和侧支循环不丰富组，ASITN/SIR分级3～4级表示侧支循环丰富，0～2级表示侧支循环不丰富。HIR定义为脑血流达峰时间(Tmax)＞10 s体积与Tmax＞6 s体积的比值^[²⁰^]。其中Tmax＞6 s体积与Tmax＞10 s体积均由自动化软件RAPID (iSchemia View，版本号：5.0.2)对灌注数据进行可视化处理与分析后生成。

1.4 统计学分析

本研究所有数据均由软件IBM SPSS Statistics 25.0生成。计数资料以频数和百分率表示，组间比较采用χ²检验；计量资料(符合正态分布)以x¯±s表示，组间比较采用独立样本t检验。由2名具有5年以上工作经验的影像科主治医师分别对DSA和TWIST图像的侧支循环分级进行评分。Kappa系数用于分析侧支循环分级在不同观察者间的一致性。Spearman秩相关系数用于分析HIR与TWIST图像的侧支循环分级的相关性。P＜0.05为差异有统计学意义。

2 结果

2.1 磁共振TWIST与DSA图像的侧支循环分级结果比较

研究期间共纳入28例急性缺血性卒中患者。磁共振TWIST (Kappa=0.826)和DSA (Kappa=0.856)图像的侧支循环分级在不同观察者间均具有高度一致性。磁共振TWIST和DSA图像的侧支循环分级结果组间差异无统计学意义(χ²=0.865，P=0.929) (表1)。图1、2分别显示了一例侧支循环丰富和侧支循环不丰富病例的PWI、磁共振TWIST和DSA图像。

点击查看大图

图1 男，56岁，急性缺血性卒中患者，左侧肢体乏力4 h入院。PWI图像(1A)显示HIR=0.0；磁共振TWIST动脉期(1B)、静脉期(1C)和静脉晚期(1D)图像显示右侧大脑中动脉闭塞，静脉期以前可见完全的侧支循环形成，侧支循环丰富，ASITN/SIR分级为4级；DSA早期造影(1E)和晚期造影(1F)图像显示右侧大脑中动脉闭塞(箭头)，侧支循环丰富(虚线圆圈)，ASITN/SIR分级为4级。注：PWI：灌注加权成像；HIR：低灌注强度比值；TWIST：时间分辨交叉随机轨迹显像；ASITN/SIR：美国介入与治疗神经放射学学会/介入放射学学会；DSA：数字减影血管造影。
图2 男，78岁，急性缺血性卒中患者，右侧肢体乏力8h入院。PWI图像(2A)显示HIR=0.7，磁共振TWIST动脉期(2B)、静脉期(2C)和静脉晚期(2D)图像显示左侧颈内动脉末端闭塞，在任何时相内，在缺血区域内没有或仅有少量软脑膜侧支，侧支循环不丰富，ASITN/SIR分级为0级；DSA早期造影(2E)和晚期造影(2F)图像显示左侧颈内动脉末端闭塞(箭头)，侧支循环不丰富，ASITN/SIR分级为0级。注：PWI：灌注加权成像；HIR：低灌注强度比值；TWIST：时间分辨交叉随机轨迹显像；ASITN/SIR：美国介入与治疗神经放射学学会/介入放射学学会；DSA：数字减影血管造影。
Fig. 1 Male, 56 years old, with acute ischemic stroke and left limb weakness for 4 h. Perfusion weighted imaging (PWI) image (1A) showed that hypoperfusion intensity ratio (HIR) was 0.0. Time-resolved with interleaved stochastic trajectories (TWIST) arterial phase (1B), venous phase (1C) and late venous phase (1D) images showed right middle cerebral artery occlusion. Complete collateral circulation was formed before venous phase, and the collateral circulation was abundant. The scores of American Society of Interventional and Therapeutic Neuroradiology/Society of Interventional Radiology (ASITN/SIR) was 4. Digital subtraction angiography (DSA) early angiography (1E) and late angiography (1F) images showed right middle cerebral artery occlusion (arrow) and abundant collateral circulation (dotted circle). The scores of ASITN/SIR was 4.
Fig. 2 Male, 78 years old, with acute ischemic stroke and right limb weakness for 8 h. Perfusion weighted imaging (PWI) image (2A) showed that hypoperfusion intensity ratio (HIR) was 0.7. Time-resolved with interleaved stochastic trajectories (TWIST) arterial phase (2B), venous phase (2C) and late venous phase (2D) images showed left internal carotid artery end occlusion. In any phase, there were no or only a few pial collateral branches in the ischemic area, and the collateral circulation was insufficient. The scores of American Society of Interventional and Therapeutic Neuroradiology/Society of Interventional Radiology (ASITN/SIR) was 0. Digital subtraction angiography (DSA) early angiography (2E) and late angiography (2F) images showed left internal carotid artery end occlusion and insufficient collateral circulation. The scores of ASITN/SIR was 0.

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表1 磁共振TWIST和DSA图像的侧支循环量化分级结果比较
Tab. 1 Comparison of quantitative classification results of collateral circulation between magnetic resonance TWIST and DSA images

2.2 两组患者一般临床资料和HIR比较及相关性分析

与侧支循环不丰富组(15例)相比，侧支循环丰富组(13例) HIR更低(0.30±0.08 vs. 0.43±0.06，P＜0.001)，其他临床资料差异均无统计学意义(P＞0.05) (表2)。相关分析显示HIR与TWIST图像的侧支循环分级呈负相关(r=-0.882，P＜0.001) (图3)。

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图3 TWIST图像的ASITN/SIR分级与HIR相关性散点图。TWIST：时间分辨交叉随机轨迹显像；ASITN/SIR：美国介入与治疗神经放射学学会/介入放射学学会；HIR：低灌注强度比值。
Fig. 3 Scatter diagram of correlation between ASITN/SIR and HIR of TWIST images. TWIST: time-resolved with interleaved stochastic trajectories; ASITN/SIR: American Society of interventional and Therapeutic Neuroradiology/Society of Interventional Radiology; HIR: hypoperfusion intensity ratio.

点击查看表格

表2 侧支循环丰富组(3～4级)与侧支循环不丰富组(0～2级)各参数之间比较
Tab. 2 Comparison of parameters between abundant collateral circulation group (score 3-4) and insufficient collateral circulation group (score 0-2)

3 讨论

本研究通过TWIST技术与DSA和HIR在评估侧支循环上的对比研究，首次系统地将TWIST技术应用于评价急性缺血性卒中患者的侧支循环，结果显示，磁共振TWIST和DSA图像的侧支循环分级结果组间差异无统计学意义；与侧支循环不丰富组相比，侧支循环丰富组HIR更低，且HIR与TWIST图像的侧支循环分级呈负相关。

3.1 磁共振TWIST与DSA图像的侧支循环分级结果分析

TWIST技术作为一种非侵入性的时间分辨4D MRA技术，通过改变K空间采集方式(由K空间全采集转变为K空间中心填充采集)、应用半傅里叶采集以及兼容并行成像技术GRAPPA，从而获得亚秒级的3D采集图像，实现了比其他动态扫描方法更高的时间分辨率^[²¹^,²²^]。这种图像采集方式不仅可获得X，Y，Z三轴的3D-MRA图像，加之有足够的时间分辨率，而且可以在原有的三轴基础上加上时间轴变量，得到多组不同时相的3D-MRA，即4D-MRA。本研究结果显示，磁共振TWIST和DSA图像的侧支循环分级结果组间差异无统计学意义。TWIST技术平均1.5 s左右采集1期图像，仅需1 min左右即可连续获得41期图像，具有较高的时间分辨率和明显的动静脉时相。TWIST技术不需要测试扫描延迟时间，即无需判断对比剂到达峰值的时间，克服了CE-MRA的扫描计时需求，彻底解决了静脉污染问题，检查成功率较高^[²³^]；生成从动脉早期到静脉晚期的血管造影图像，其动态效果可以与DSA相媲美，有利于对血管病变的评估^[²⁴^,²⁵^]。Parmar等^[²⁶^]研究显示，使用4D-MRA对头颈部血管进行造影检查，能够可视化血管增强的动脉期、静脉期和静脉晚期影像，获得解剖学和时间信息，类似于DSA的检查效果，但没有电离辐射暴露、碘化对比剂过敏或导管插入致动脉损伤等风险。Roh等^[¹⁶^]对67例由单侧颈内动脉或大脑中动脉M1段狭窄闭塞病变引起的急性缺血性卒中患者的TWIST和动态磁敏感对比增强磁共振灌注(dynamic susceptibility contrast-enhanced magnetic resonance perfusion, DSC-MRP)数据进行分析，利用TWIST和DSC-MRP的动态信号分别生成多相MRA侧支图和MRP侧支图，通过与DSC-MRP衍生的多相侧支成像方法(MRP侧支图)进行比较，验证TWIST的多相MRA侧支图作为侧支成像方法的应用价值。结果显示，多相MRA侧支图和MRP侧支图对于侧支循环分级具有良好一致性。研究表明，磁共振TWIST生成的多相MRA侧支图可以提供可靠的侧支信息，是急性缺血性卒中患者侧支循环成像的一种可行性方法。

3.2 TWIST图像的侧支循环与HIR的相关性分析

前期研究显示，HIR可以提示脑组织内低灌注严重程度和侧支血流，是MRA侧支循环的可靠指标，可作为评估侧支循环以及判断患者是否可行静脉溶栓或机械取栓治疗的可行性指标等^[²⁷^,²⁸^]。本研究根据TWIST图像的侧支循环分级将患者分为侧支循环丰富组和侧支循环不丰富组，ASITN/SIR分级3～4级表示侧支循环丰富，0～2级表示侧支循环不丰富。本研究结果显示，与侧支循环不丰富组相比，侧支循环丰富组HIR更低，且HIR与TWIST图像的侧支循环分级呈负相关。徐佳等^[²⁹^]研究显示低HIR与丰富的侧支循环密切相关，HIR＜0.4是预测急性缺血性卒中患者良好侧支循环的最佳临界值。Guenego等^[³⁰^]研究显示HIR与DSA的侧支循环分级呈负相关，HIR＜0.4是预测良好侧支循环的最佳临界值。Lyndon等^[³¹^]研究显示HIR与CT血管造影的侧支循环分级呈负相关，HIR对于卒中治疗前侧支循环评估具有重要的指导意义，这与本研究的结果一致。

3.3 局限性

本研究有一定的局限性：(1)本研究纳入的不同级别侧支循环样本量较少且不对等，可能会在一定程度上影响研究结果的可信度，会在后续研究中进一步加大样本量，以验证该研究；(2)血管欠清晰，这也是TWIST序列的一个特征表现，未来对于优化TWIST参数的前瞻性研究将有助于进一步评估。

综上所述，磁共振TWIST技术可以无创、快速地提供动态信息并连续、稳定地完成纯动静脉时相成像，能够实现急性缺血性卒中的无创侧支循环成像，在侧支循环诊断中具有较高的价值，有助于临床治疗决策的制订。

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