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临床研究
基于低灌注强度比值的侧支循环对晚期时间窗急性脑卒中预后预测的研究
陈乾 彭明洋 王同兴 陈国中 殷信道 任军

Cite this article as: CHEN Q, PENG M Y, WANG T X, et al. A study on predicting the outcome of acute stroke in late-time windows using collateral circulation based on hypoperfusion intensity ratio[J]. Chin J Magn Reson Imaging, 2024, 15(7): 76-80, 93.本文引用格式:陈乾, 彭明洋, 王同兴, 等. 基于低灌注强度比值的侧支循环对晚期时间窗急性脑卒中预后预测的研究[J]. 磁共振成像, 2024, 15(7): 76-80, 93. DOI:10.12015/issn.1674-8034.2024.07.013.


[摘要] 目的 以急性脑卒中患者数字减影血管造影(digital subtraction angiography, DSA)为侧支循环标准,探讨低灌注强度比值(hypoperfusion intensity ratio, HIR)在晚期时间窗急性脑卒中患者血管内治疗后预后的预测价值。材料与方法 回顾性分析2020年1月至2023年3月在本院行血管内治疗的晚期时间窗(6~24 h)急性脑卒中患者160例,侧支循环评分采用美国介入和治疗神经放射学会(American Society of Interventional and Therapeutic Neuroradiology, ASITN)分级系统评估(侧支循环良好:3~4级;侧支循环不良:0~2级)。HIR为脑血流达峰时间(time-to-maximum, Tmax)>10 s体积与Tmax>6 s体积的比值。3个月预后采用改良Rankin量表(modified Rankin Scale, mRS)评分评估(预后良好:0~2分;预后不良:3~6分)。应用Spearman等级相关分析及受试者工作特征(receiver operating characteristic, ROC)曲线分析HIR与侧支循环间的相关性及其在晚期时间窗急性脑卒中患者预后中的预测价值。结果 与侧支循环良好组(n=90)相比,侧支循环不良组(n=70)的HIR值较高(0.45±0.07 vs. 0.30±0.08;P<0.001)、出血转化率较高(44.43% vs. 20.00%;P=0.003)、早期神经功能恶化率较高(45.71% vs. 23.33%;P=0.003)及预后良好率较低(44.29% vs. 67.78%;P=0.030)。Spearman相关分析显示HIR值与ASITN分级间具有良好的负相关(预后良好组:r=-0.856;P<0.001;预后不良组:r=-0.888;P<0.001);HIR值与3个月mRS评分具有良好的正相关(r=0.773;P<0.001)。多因素logistic回归分析显示HIR [OR(95% CI):0.629(0.421~1.418);P=0.041]为晚期时间窗急性脑卒中EVT治疗后预后的独立预测因子。ROC曲线分析显示ASITN分级与HIR预测晚期时间窗急性卒中预后的预测效能差异无统计学意义(AUC:0.837 vs. 0.887;Z=1.696,P=0.090)。结论 基于HIR的侧支循环评估可准确晚期时间窗急性脑卒中血管内治疗后预后,为临床提供个性化治疗方案指导。
[Abstract] Objective To explore the predictive value of hypoperfusion intensity ratio (HIR) in the outcome of late-time windows acute stroke patients after endovascular thrombectomy, using digital subtraction angiography (DSA) as collateral circulation standard.Materials and Methods A total of 160 acute stroke patients in late-time windows (6-24 hours) receiving endovascular thrombectomy therapy in our study from January 2020 to March 2023 were analyzed retrospectively. American Society of Interventional and Therapeutic Neuroradiology (ASITN) grading system was used to evaluate the collateral circulation (poor collateral circulation: 0-2 grade; good collateral circulation: 3-4 grade). HIR was defined as the ratio of the time-to-maximum (Tmax)>10 s over Tmax>6 s lesion volumes. Modified Rankin Scale (mRS) score was used to evaluate the outcome at 3 months (good outcome: 0-2 score; poor outcome: 3-6 score). Spearman rank correlation and receiver operating characteristic (ROC) curve analysis were performed to evaluate the predictive value in the outcome of acute stroke patients in the late-time windows.Results Compared with the good collaterals group (n=90), the poor collaterals group (n=70) had higher HIR values (0.45±0.07 vs. 0.30±0.08; P<0.001), higher hemorrhagic transformation rates (44.43% vs. 20.00%; P=0.003), higher early neurological deterioration rates (45.71% vs. 23.33%; P=0.003), and lower good outcome rates (44.29% vs. 67.78%; P=0.030). Spearman correlation analysis showed good negative correlation between HIR value and ASITN grading (good outcome group: r=-0.856; P<0.001; poor outcome group: r=-0.888; P<0.001); the HIR value is positively correlated with the mRS score at 3 month (r=0.773; P<0.001). Multivariate logistic regression analysis showed that HIR [OR (95% CI): 0.629 (0.421-1.418); P=0.041] is independent predictors of time from stroke onset. ROC curve analysis showed that there was no significant statistical difference in the predictive efficacy of ASITN grading and HIR in predicting the outcome of acute stroke in the late-time window (AUC: 0.837 vs. 0.887; Z=1.696, P=0.090).Conclusions The evaluation of collateral circulation based on HIR can accurately predict the outcome after endovascular treatment of acute stroke in the late-time windows, providing personalized treatment guidance for clinical practice.
[关键词] 卒中;磁共振成像;灌注成像;预后;晚期时间窗
[Keywords] stroke;magnetic resonance imaging;perfusion imaging;outcome;late-time windows

陈乾    彭明洋    王同兴    陈国中    殷信道    任军 *  

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:任军,E-mail:renjun1203@163.com

作者贡献声明:任军设计本研究的方案,对稿件重要内容进行了修改;陈乾起草和撰写稿件,获取、分析和解释本研究的数据;彭明洋、王同兴、陈国中、殷信道获取、分析或解释本研究的数据,对稿件重要内容进行了修改,其中陈国中获得了国家自然科学基金项目和中国博士后科学基金项目的资助;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: 国家自然科学基金项目 82001811 中国博士后科学基金项目 2022M711664
收稿日期:2023-12-18
接受日期:2024-06-03
中图分类号:R445.2  R743.3 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2024.07.013
本文引用格式:陈乾, 彭明洋, 王同兴, 等. 基于低灌注强度比值的侧支循环对晚期时间窗急性脑卒中预后预测的研究[J]. 磁共振成像, 2024, 15(7): 76-80, 93. DOI:10.12015/issn.1674-8034.2024.07.013.

0 引言

       侧支循环决定脑缺血发展速度及严重程度,可区分患者脑缺血进展快慢及评估相应的治疗机会[1, 2]。急性脑卒中治疗前评估侧支循环对患者临床治疗方案的选择至关重要[3, 4]。研究显示,具有良好侧支循环的急性卒中患者对静脉溶栓治疗和血管内机械取栓(endovascular thrombectomy, EVT)治疗效果更好,病变进展更慢和预后更好[5, 6]。然而,以往的研究多为早期治疗窗口(发病时间6 h以内)的急性脑卒中患者,而晚期时间窗口(发病时间> 6 h)的患者其侧支循环与预后的关系研究较少。低灌注强度比值(hypoperfusion intensity ratio, HIR)作为侧支循环的评估指标,可进行快速、无创的评估[7, 8]。目前基于HIR作为侧支循环评估晚期时间窗的急性脑卒中患者预后的价值尚无报道。本研究旨在以数字减影血管造影(digital subtraction angiography, DSA)为金标准,基于HIR的侧支循环指标探讨其在晚期时间窗急性脑卒中患者EVT治疗后预后的预测价值。

1 材料与方法

1.1 研究对象

       本研究遵守《赫尔辛基宣言》,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。回顾性分析2020年1月至2023年3月在本院神经内科就诊的急性缺血性脑卒中患者临床及影像资料。纳入标准:(1)首发卒中;(2)发病时间为6~24 h;(3)入院后行MRI检查;(4)接受DSA造影且进行EVT治疗。排除标准:(1)颅内存在出血、肿瘤或创伤等影响预后评估的疾病;(2)DSA影像无法评估侧支循环;(3)MRI有运动伪影图像无法评估。共160例,其中男100例,女60例,年龄(70.11±17.45)岁。收集患者的基线资料[性别、年龄、入院美国国立卫生研究院卒中量表(National Institute of Health Stroke Scale, NIHSS)评分)、急性脑卒中发病相关的高危因素(高血压、糖尿病、高血脂、高同型半胱氨酸、房颤)、发病至MRI检查时间、发病至EVT时间]。早期神经功能恶化定义为EVT后24 h内NIHSS评分持续增加≥2分或死亡[9]。出血转化定义为EVT后24 h内头颅CT或MRI复查存在脑实质出血或蛛网膜下腔出血[10]。3个月预后采用改良Rankin量表(modified Rankin Scale, mRS)评分进行评估:0~2分为预后良好;3~6分为预后不良[11]

1.2 检查方法

       采用3.0 T MR扫描设备(Magnetom Prisma, Siemens Healthineer, Germany)进行治疗前MRI检查。MRI扫描序列包括液体衰减反转恢复序列、弥散加权成像(diffusion weighted imaging, DWI)、磁共振血管造影(magnetic resonance angiography, MRA)、灌注加权成像(perfusion weighted imaging, PWI)。DWI选用自旋回波序列序列,扫描参数如下:TR 2600 ms,TE 98 ms,翻转角90°,视野220 mm×220 mm,矩阵224×224,层厚6 mm,16层,层间距1.3 mm,b=0、1000 s/mm2;动态对比增强MRA选用梯度回波脉冲序列,扫描参数如下:TR 20 ms,TE 3.3 ms,视野220 mm×220 mm,矩阵528×531,层厚0.60 mm,持续时间58秒。动态磁敏感对比增强-PWI选用梯度回波-平面回波序列,扫描参数如下:TR 1500 ms,TE 30 ms,翻转角90°,视野220 mm×220 mm,矩阵128×128,层厚4 mm,20层,持续时间88 s。采用Medtron公司双流高压注射器Accutron MR经右侧肘前静脉给药钆喷酸葡胺(Gd-DTPA,广州康辰药业有限公司;浓度:0.05 mmol/kg;流速:4 mL/s)后扫描,每个定位扫描60次。

1.3 影像分析

       DWI梗死体积、Tmax>6 s体积及Tmax>10 s体积均由RAPID软件自动生成。HIR=Tmax>10 s体积/Tmax>6 s体积[12]。侧支循环金标准采用美国介入和治疗神经放射学会(American Society of Interventional and Therapeutic Neuroradiology, ASITN)分级系统在DSA图像上进行评估(0=无侧支循环血流达到缺血区域-4=血流快速而完全地灌注到整个梗死区域),ASITN分级0~2级定义为侧支循环不良,ASITN分级3~4级定义为侧支循环良好[13]。由2位有10年工作经验的神经放射学诊断副主任医师采用双盲法对所有影像资料进行分析,结果不一致时经协商后达成一致。

1.4 统计学分析

       应用SPSS 19.0统计学软件进行数据处理。计量资料采用均数±标准差表示,计数资料采用例(%)表示。采用独立t检验或卡方检验对资料进行统计学分析。应用Spearman等级相关分析HIR与ASITN分级之间、HIR与3个月预后之间的相关性。应用单因素和多因素logistic回归分析确定晚期时间窗急性脑卒中EVT治疗后预后的独立影响因子,计算优势比(odds ratio, OR)及其95%可信区间(confidence interval, CI)。应用受试者工作特征(receiver operating characteristic, ROC)曲线分析HIR在预测晚期时间窗急性脑卒中EVT治疗后预后中的价值,确定最佳临界值及其敏感度和特异度。P<0.05为差异有统计学意义。

2 结果

2.1 侧支循环良好(ASITN 3~4级)与侧支循环不良(ASITN 0~2级)各参数之间比较

       共160例患者纳入分析,其中侧支循环良好(ASITN 3~4级)患者90例、侧支循环不良(ASITN 0~2级)患者70例。与侧支循环良好组相比,侧支循环不良组的治疗前DWI梗死体积较大(42.96±14.75 vs. 30.34±10.17;P=0.031)、PWI-DWI不匹配体积较大(99.34±16.61 vs. 74.21±11.85;P=0.015)及HIR值较高(0.45±0.07 vs. 0.30±0.08;P<0.001)(图12)。经EVT治疗后,侧支循环不良组出血转化率(44.43% vs 20.00%)及早期神经功能恶化率(45.71% vs. 23.33%)较侧支循环良好组高,差异有统计学意义(P<0.05)。3个月预后随访显示侧支循环不良组的预后良好发生率为44.29%,侧支循环良好组发生率为67.78%,两组间比较差异有统计学意义(P=0.030)(表1)。

图1  男,63岁,因“右侧肢体乏力9 h”入院。入院DWI(1A)示左侧岛叶急性脑卒中,PWI(1B)示HIR为0.2,DSA造影(1C)示左侧大脑中动脉闭塞,ASITN分级为4分。行血管内治疗后3个月预后mRS评分为1分,预后良好。
图2  女,64岁,因“右侧肢体乏力7 h”入院。入院DWI(2A)示左侧基底节区及左侧颞叶急性脑卒中,PWI(2B)示HIR为0.5,DSA造影(2C)示左侧大脑中动脉闭塞,ASITN分级为1分。行血管内治疗后3个月预后mRS评分为4分,预后不良。DWI:扩散加权成像;PWI:灌注加权成像;HIR:低灌注强度比值;DSA:数字减影血管造影;ASITN:美国介入和治疗神经放射学会;mRS:改良Rankin量表。
Fig. 1  Male, 63 years old, right limb weakness for 9 h. DWI on admission (1A) shows that acute stroke in left insular, PWI (1B) shows that HIR is 0.2, DSA (1C) shows that the left middle cerebral artery is occluded, and ASITN is 4 points. After 3 months of endovascular treatment, the mRS score is 1, indicating a good outcome.
Fig. 2  Female, 64 years old, right limb weakness for 7 h. DWI on admission (2A) shows that acute stroke in left basal ganglia and left temporal lobe, PWI (2B) shows that HIR is 0.5, DSA (2C) shows that the left middle cerebral artery is occluded, and ASITN is 1 point. After 3 months of endovascular treatment, the mRS score is 4, indicating a poor outcome. DWI: diffusion-weighted imaging; PWI: perfusion-weighted imaging; HIR: hypoperfusion intensity ratio; DSA: digital subtraction angiography; ASITN: American Society of Interventional and Therapeutic Neuroradiology; mRS: modified Rankin Scale.
表1  晚期时间窗急性脑卒中患者侧支循环良好组与侧支循环不良各参数之间比较
Tab. 1  Comparison of parameters between good collateral circulation and poor collateral circulation in acute stroke patients in late-time windows

2.2 HIR与ASITN分级间、3个月mRS评分间相关性分析

       Spearman相关分析显示HIR值与ASITN分级间具有较强的负相关(r=-0.805,P<0.001)(图3A)。进一步分层分析显示无论在预后良好组还是预后不良组,HIR值与ASITN分级间均具有良好的负相关(预后良好组:r=-0.856,P<0.001;预后不良组:r=-0.888,P<0.001)(图3B)。HIR值与3个月mRS评分具有良好的正相关(r=0.773,P<0.001)(图3C)。

图3  晚期时间窗急性脑卒中患者HIR与ASITN分级(3A)、亚组患者HIR与ASITN分级(3B)、3个月mRS评分与HIR(3C)相关性散点图。HIR:低灌注强度比值;ASITN:美国介入和治疗神经放射学会;mRS:改良Rankin量表。
图4  HIR、ASITN分级预测晚期时间窗急性脑卒中患者预后的ROC曲线分析。HIR:低灌注强度比值;ASITN:美国介入和治疗神经放射学会;ROC:受试者工作特征。
Fig. 3  Scatter diagram of correlation between HIR and ASITN grading (3A), HIR and ASITN grading in subgroup (3B), mRS at 3 months and HIR (3C) in acute stroke patients in the late-time windows. HIR: hypoperfusion intensity ratio; ASITN: American Society of Interventional and Therapeutic Neuroradiology; mRS: modified Rankin Scale.
Fig. 4  ROC curve analysis of HIR and ASITN grading in predicting outcome in acute stroke patients in the late-time windows. HIR: hypoperfusion intensity ratio; ASITN: American Society of Interventional and Therapeutic Neuroradiology; ROC: receiver operating characteristic.

2.3 单因素及多因素logistic回归分析

       以3个月预后为因变量进行单因素及多因素logistic回归分析,在单因素logistic回归分析中,治疗前DWI梗死体积[OR(95% CI):0.732(0.531~1.128);P=0.04]、PWI-DWI不匹配体积[OR(95% CI):0.535(0.356~1.211);P=0.035]及HIR [OR(95% CI):0.714 (0.415~1.521);P=0.021)与晚期时间窗急性脑卒中EVT治疗后预后密切相关。进一步多因素logistic回归分析显示,HIR [OR(95% CI):0.629(0.421~1.418);P=0.041]为晚期时间窗急性脑卒中EVT治疗后预后的独立预测因子。

2.4 侧支循环预测晚期时间窗急性脑卒中预后的价值

       ROC曲线分析(图4)显示ASITN分级预测晚期时间窗急性脑卒中患者预后的曲线下面积(area under the curve, AUC)为0.837(95% CI:0.773~0.901)。当ASITN分级的最佳临界值为2.5时,预测卒中预后的敏感度和特异度分别为76%和77%。HIR预测晚期时间窗急性脑卒中患者预后的AUC为0.887(95% CI:0.837~0.936)。当HIR的最佳临界值为0.25时,预测卒中预后的敏感度和特异度分别为96%和75%。经DeLong检验显示两个模型间差异无统计学意义(Z=1.696,P=0.090)。

3 讨论

       本研究通过对160例晚期时间窗的急性脑卒中患者的侧支循环分析显示,具有良好侧支循环的患者其核心梗死体积较小,在EVT治疗后其出血转化发生率较低,早期神经功能恶化发生率较低,预后良好率较高。基于HIR的侧支循环为预后的独立预测因子,可准确预测晚期时间窗急性脑卒中患者EVT治疗后预后,其AUC可达0.887。与金标准DSA相比,HIR是一个可靠的侧支循环评估指标,可为临床预后评估、治疗方案制订提供帮助。

3.1 侧支循环在晚期时间窗急性脑卒中中的价值

       已有较多的研究报道丰富的侧支循环是急性脑卒中静脉溶栓或血管内治疗后预后的预测指标[14, 15, 16]。侧支循环可以维持梗死核心区周围的血液循环,是决定急性脑卒中后最终梗死体积和缺血半暗带的主要因素,与卒中预后密切相关[17, 18, 19]。先前的研究已显示了大血管闭塞的患者静脉溶栓后再通与侧支循环密切相关。类似地,在早期时间窗的大血管闭塞患者治疗的研究中(MR CLEAN随机对照试验、SWIFT试验)发现良好的侧支循环对EVT治疗的影响最大[20, 21, 22]。然而,最近对DEFUSE-3试验的分析发现在晚期时间窗的患者中并未发现这一影响[23, 24]。DEFUSE-3试验显示,尽管良好的侧支循环与较小的梗死体积相关,但侧支循环无法预测临床预后。本研究结果显示晚期时间窗的急性脑卒中患者,当侧支循环丰富时,其梗死体积通常较小,早期神经功能恶化率较低,出血转化率较低及预后较好。本研究与DEFUSE-3试验结果不一致的可能原因为:DEFUSE-3试验的未再灌注治疗的患者侧支循环不良较多、不良侧支循环的比例较低及由侧支循环保护的大脑功能区域相关性决定。LIEBESKIND等[25]研究显示无论在CT血管造影还是DSA,侧支循环丰富的晚期时间窗急性脑卒中患者通常具有较小的梗死体积和较好的预后,本研究结果与LIEBESKIND等的类似。这些结果强调了晚期时间窗患者侧支循环的重要性,它是治疗效果和长期神经功能预后的有力预测指标。

3.2 基于HIR的侧支循环在晚期时间窗急性脑卒中预后评估中的价值

       DSA虽是评估脑血管病变侧支循环的“金标准”,然而,其有创性严重限制了DSA技术在临床上的常规使用[26, 27, 28]。灌注成像作为急性脑卒中重要的影像评估手段,在脑卒中时间窗内尤其是超时间窗患者治疗的筛选中起着非常重要的作用。其中Tmax作为缺血半暗带的重要评估参数,其延迟的病变与临床恢复密切相关[29, 30, 31]。HIR为基于Tmax计算得出的用于评估脑卒中内侧支血流的指标,被认为与侧支循环程度相关[32, 33, 34]。本研究以DSA侧支循环为标准,探讨HIR在晚期时间窗患者中评估侧支循环的准确性,结果显示HIR与侧支循环高度相关。以往已有较多研究显示HIR是一个有价值的基于灌注的侧支循环稳定性指标,可作为在EVT治疗前评估侧支循环的有力工具。本研究以HIR作为侧支循环的指标,进一步预测晚期时间窗急性脑卒中患者EVT治疗后预后,结果显示HIR预测卒中预后的AUC为0.887,其敏感度和特异度分别为96%和75%。Tmax>6 s病变包括了大部分延迟时间大于8~10 s的不同程度低灌注组织,而组织的低灌注严重程度和持续时间决定了缺血组织的命运[35]。此外,本研究结果还显示ASITN分级预测晚期时间窗急性脑卒中预后的AUC为0.837,其敏感度和特异度分别为76%和77%。与HIR预测卒中预后的效能无明显差异,这是本研究的创新点。灌注成像已在急性缺血性脑卒中中广泛使用,使用自动软件(RAPID)计算HIR方便、快捷、无创,可消除不同观察者评估存在的潜在差异。由此可见,应用HIR代替DSA作为侧支循环的无创评估指标仍然可准确预测晚期时间窗急性脑卒中患者的预后。

3.3 局限性

       本研究尚存在一定的局限性。本研究为回顾性研究,为使侧支循环良好组和不良组相对均衡,本研究在样本选择时存在一定的偏倚。其次,本研究所采用的侧支循环及影像学变量评估方法可能在大部分医院无法实施,这也是本研究的局限性之一。此外,本研究为单中心研究,需进一步进行多中心验证。

4 结论

       综上所述,HIR与良好的侧支循环高度相关,基于HIR的侧支循环指标可准确预测晚期时间窗急性脑卒中EVT治疗后早期神经功能恶化、出血转化及预后,为临床个性化治疗方案制订提供帮助。

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