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综述
多模态MRI对急性缺血性脑卒中诊断及预后评估的研究进展
秦元林 于昊 陈月芹

Cite this article as: Qin YL, Yu H, Chen YQ. Research progress of multimodal MRI in the diagnosis and prognosis assessment of acute ischemic stroke[J]. Chin J Magn Reson Imaging, 2022, 13(8): 112-116.本文引用格式:秦元林, 于昊, 陈月芹. 多模态MRI对急性缺血性脑卒中诊断及预后评估的研究进展[J]. 磁共振成像, 2022, 13(8): 112-116. DOI:10.12015/issn.1674-8034.2022.08.025.


[摘要] 急性缺血性脑卒中(acute ischemic stroke, AIS)发病率逐年上升,已成为世界范围内的第二大死因以及导致永久性残疾的主要原因。多模态MRI以其多参数、多序列成像等优势对病变进行综合评估,为患者诊断、治疗方式的选择、预后的评估提供重要依据。近年来,MRI预测AIS预后与转归成为研究热点,本文就多模态MRI在AIS诊断及预后评估中的研究进展进行综述。
[Abstract] The incidence of acute ischemic stroke (AIS) is rising gradually and has become the second common cause of death worldwide and the leading cause of permanent disability. Multimodal magnetic resonance imaging provides useful information for diagnosis, treatment choice, and prognosis assessment through comprehensive evaluation by multi-parameter and multi-sequence imaging. In recent years, MRI technique to predict prognosis and outcome of AIS has become a research hotspot. This review summarizes the progress of multimodal MRI in the diagnosis and prognosis assessment of acute ischemic stroke.
[关键词] 急性缺血性脑卒中;诊断;预后;磁共振成像;磁敏感加权成像;灌注加权成像;酰胺质子转移
[Keywords] acute ischemic stroke;diagnosis;prognosis;magnetic resonance imaging;susceptibility weighted imaging;perfusion weighted imaging;amide proton transfer

秦元林 1   于昊 2   陈月芹 2*  

1 济宁医学院临床医学院,济宁 272013

2 济宁医学院附属医院医学影像科,济宁 272029

陈月芹,E-mail:chenyueqin010@163.com

作者利益冲突声明:全体作者均声明无利益冲突。


基金项目: 国家自然科学基金 82001805
收稿日期:2022-04-16
接受日期:2022-08-10
中图分类号:R445.2  R743.3 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2022.08.025
本文引用格式:秦元林, 于昊, 陈月芹. 多模态MRI对急性缺血性脑卒中诊断及预后评估的研究进展[J]. 磁共振成像, 2022, 13(8): 112-116. DOI:10.12015/issn.1674-8034.2022.08.025

       脑卒中是指多种原因引起的脑部血管突然破裂或血管栓塞造成血液不能流入大脑所致局限性或全面性脑组织损伤的一组疾病。急性缺血性脑卒中(acute ischemic stroke, AIS)是我国最常见的卒中类型,约占我国脑卒中的70%,因其高发病率、高致残率和高病死率的特点,已造成严重的社会和经济负担。早期诊断、早期治疗对改善患者预后具有重大意义。近年来,随着诊疗技术的进步,对于一部分发病时间超出传统时间窗的患者也可以从再灌注治疗中获益[1, 2]。多模态MRI可以通过多序列、多参数对脑实质、脑血管、脑血流动力学情况进行综合评估,准确反映AIS患者的病理生理状态,进而为患者诊疗计划的制订与预后效果的评估提供合理的证据与指导。本文就多模态MRI在AIS诊断及预后评估中的研究进展进行综述。

1 T2液体衰减反转恢复序列

       T2液体衰减反转恢复(T2 fluid attenuated inversion recovery, T2-FLAIR)序列是颅脑MRI检查中的常规序列,可以抑制自由水信号并产生重T2加权像,在AIS的诊断、评估发病时间、预后预测中发挥重要作用。研究表明FLAIR-扩散加权成像(diffusion-weighted imaging, DWI)不匹配提示发病时间小于4.5 h[3, 4],可以作为静脉溶栓治疗的证据。此外,在部分AIS患者FLAIR序列中可以发现FLAIR血管高信号征(FLAIR vascular hyperintensity, FVH),即位于蛛网膜下腔的点状、条状或管状高信号。一般认为FVH的形成与缺血区血流缓慢有关,可以用于评估大血管闭塞(large vessel occlusion, LVO)、侧支循环、组织灌注及临床预后[5]。Legrand等[6]发现FVH-DWI不匹配可以作为评估缺血半暗带的替代方法。FVH作为预测AIS预后与转归的影像标记物成为研究热点,然而FVH与预后的相关性存在争议,究其原因为FVH受众多因素影响,比如时间、梗死模式、血管受累程度等[7, 8, 9]。有研究发现FVH征可提示接受再灌注治疗的急性大血管闭塞性缺血性卒中(AIS-LVO)患者预后良好。Jiang等[10]通过研究37例AIS-LVO患者再灌注治疗前FVH1评分和再灌注治疗后FVH2评分发现预后良好组FVH1评分高于预后不良组,而FVH2评分低于后者;3个月后改良Rankin量表(modified Rankin Scale, mRS)评分与FVH1评分呈负相关而与FVH2评分呈正相关。Zhu等[11]对发病4.5 h内的190例接受静脉溶栓治疗的AIS-LVO患者研究发现FVH评分可能是预测患者预后的独立危险因素,对预后具有良好预测价值[受试者工作特诊曲线下面积(area under the curve, AUC)=0.853],并且与出院时的美国国立卫生研究院卒中量表(National Institute of Health Stroke Scale, NIHSS)评分和第1、3、6个月时mRS评分呈显著负相关。然而部分研究报道FVH与未接受再灌注治疗患者的不良预后相关,Kim等[12]研究发现对于未接受再灌注治疗的AIS患者,FVH可能是预后不良的独立预测因素。近期也有学者将深度学习方法应用到研究之中[3],通过深度学习方法提取DWI序列信息合成FLAIR图像,该图像与FLAIR序列获取的图像相关性良好,从而可以缩短AIS患者扫描时间,但其价值还需前瞻性多中心试验进一步验证。

2 磁共振血管成像

       颅脑磁共振血管成像(magnetic resonance angiography, MRA)是AIS常规检查序列,主要用于检测动脉闭塞情况及评估侧支循环。常用方法包括时间飞跃法MRA(time-of-flight MRA, TOF-MRA)和对比增强MRA(contrast enhancement MRA, CE-MRA)。TOF-MRA无需注射对比剂,在临床得以广泛开展,其对狭窄性、闭塞性病变的敏感性较高,但容易因血管解剖因素引起部分饱和效应或湍流失相位导致血流信号减低或消失,造成血管狭窄评估不准确。CE-MRA通过注射外源性对比剂,通过剪影处理增强前后图像获得血管影像。CE-MRA图像质量优于TOF-MRA,但是因需要注射外源性对比剂,可能引起肾源性系统性纤维化,对于肾功能不全患者应用受限,该方法在明确闭塞位置及评估侧支循环方面优于TOF-MRA[13, 14]。陈广浩等[15]对机械取栓治疗的AIS患者研究发现MRA侧支循环与预后相关,软脑膜侧支循环丰富提示预后相对较好。随着MRI技术的进步,血管壁成像技术逐渐应用于临床,其对动脉粥样硬化型缺血性脑卒中具有重要评估价值。高分辨血管壁MRI(high-resolution vessel wall MRI, HR-VW-MRI)可以直接显示动脉粥样硬化性斑块形态及强化程度,分析斑块成分、斑块负荷、易损性等特征,有研究[16]发现斑块强化是预测卒中发生风险的有效标记物。实际临床工作中,MRA可迅速检出血管狭窄,亦可通过评估侧支循环对预后有一定的预测价值。

3 DWI

       DWI具有扫描时间短、可重复性强、诊断效能高的特点,并可以通过表观扩散系数(apparent diffusion coefficient, ADC)定量反映组织水分子的微观运动情况,是目前AIS检出最具敏感性的检查技术,发病3 h及6 h内的检出敏感度分别达到73%~92%、95%~100%[17]。DWI是预测AIS预后的可靠影像标记物。Raoult等[18]研究发现,对于接受动脉取栓的患者,DWI所示病灶体积大于80 mL是3个月预后不良敏感性和特异性最高的独立危险预测因素;同时证明DWI病灶体积联合年龄、治疗前NIHSS评分及发病时间预测动脉取栓术后3个月功能预后的算法具有较高的预测价值。有研究[19, 20]发现接受血管内治疗的患者,患者治疗前、后DWI梗死体积及DWI梗死体积增长与3个月mRS评分均呈正相关,且对临床预后具有较高的预测价值。然而DWI存在一定可逆性,即DWI所示病变体积不能代表最终梗死体积[21]。几种先进的DWI技术如扩散张量成像(diffusion tensor imaging, DTI)、扩散峰度成像(diffusion kurtosis imaging, DKI)等已应用于AIS的评估中。DTI可以很好地反映白质纤维束走向,通过计算各向异性分数(fractional anisotropy, FA)来反映脑白质受损情况。对于AIS患者,脑白质微观结构发生变化FA值降低,随着时间推移FA值没有恢复正常则提示不可逆损伤。DTI可以通过分析不同神经束的受损情况评估AIS患者预后,比如预测运动功能及语言功能的临床恢复情况[22]。DKI是DTI的延伸,可定量分析峰度参数进而描述细胞内外水分子非高斯分布特点,能够较DWI、DTI提供更准确的组织微结构信息。Yin等[23]探讨AIS患者入院时DWI、DKI参数与发病一个月后组织预后的关系,结果发现平均峰度(mean kurtosis, MK)图所示病变体积及数目与随访(T2WI)最终梗死体积及数目的相关性显著高于DWI。虽然研究发现DKI可以更精确地评估缺血核心,然而其不同脑组织的MK本身存在差异,因此其临床可行性还需进一步研究证实[21]

4 磁敏感加权成像

       磁敏感加权成像(susceptibility weighted imaging, SWI)在T2*加权梯度回波序列的基础上同时获得相位信息及强度信息,经后处理使具有不同磁敏感性的组织对比成像[24]。SWI是检测急性卒中患者颅内出血、动脉血栓、微出血及出血性转化的有效成像方式。SWI-DWI不匹配亦可评估缺血半暗带[25, 26]。近年来,突出静脉征(prominent veins sign, PVS)、磁敏感血管征(susceptibility vessel sign, SVS)与预后的关系成为研究热点。

       PVS是SWI序列患侧大脑半球皮髓质静脉低信号较对侧增多及增粗的征象,分为显著皮质静脉征(prominent cortical veins, PCV)、不对称显著皮质静脉征(asymmetrically prominent cortical veins, APCV)和深髓质静脉征(deep medullary veins, DMV)。其形成机制和脑组织缺血缺氧与血管扩张有关。Oh等[27]报道了PCV在AIS再灌注治疗患者中的临床意义,研究发现在前循环AIS-LVO患者中,广泛PCV显影与多时相CT血管造影(multiphase CT angiography, mCTA)扫描示软脑膜侧支循环良好呈负相关;对于接受再灌注治疗的患者,PCV阳性患者血管成功再通的可能性降低约20%。APCV表现为患侧大脑半球皮质静脉数目、长度及管径均超过健侧,是AIS患者常见征象。APCV显影区域与灌注图像平均通过时间受损区域相匹配,表明APCV可以反映组织灌注减低,APCV阳性可提示预后不良[24]。Lu等[28]发现APCV的动态变化与静脉血氧饱和度相关,治疗后APCV消失提示静脉血氧饱和度增高、预后良好。DMV在SWI上表现为脑室周围白质内或垂直于侧脑室长轴的细小低信号,DMV阳性提示预后不良与APCV价值相仿[29]。PVS阳性往往提示颅内大动脉的严重狭窄或闭塞,提示病情严重、预后相对较差。

       SVS表现为闭塞血管内低信号,其直径超过对侧血管。SVS可以显示血栓形态、大小、长度[30]。Soize等[31]发现SVS阳性检出取决于从发病至成像的时间,发病时间越长,SVS阳性检出率越高。Lee等[32]报道血栓长度为支架机械取栓术再通失败的预测因子,血栓长度过长与再通成功率显著下降相关。He等[33]对临床症状轻微的AIS-LVO患者研究发现SVS所示血栓长度与早期神经功能恶化(early neurological deterioration, END)风险相关,SVS≥9.45 mm是END的独立预测因子。一项荟萃分析[34]表明SVS阳性患者接受机械取栓治疗更可能获得良好预后;而对于仅接受静脉溶栓治疗或未进行再灌注治疗的患者,SVS阳性往往提示预后不良。在临床工作中,对于符合再灌注治疗条件的SVS阳性AIS患者,应优先进行机械取栓治疗以期获得良好预后。

5 灌注加权成像

       灌注加权成像(perfusion weighted imaging, PWI)是AIS患者MRI扫描方案的重要组成部分,用于评估脑组织的缺血核心、缺血半暗带以及指导再灌注治疗。临床工作中应用较多的是注射对比剂的动态磁敏感对比增强PWI(dynamic susceptibility contrasts enhanced PWI, DSC-PWI)及无需注射对比剂的动脉自旋标记(arterial spin labeling, ASL)。PWI是评估组织窗的最佳检查方式之一。近年来,随着大型临床队列研究成果相继发表,再灌注治疗的选择标准越来越重视组织窗的评估[1, 2]

       DSC-PWI是通过静脉快速团注顺磁性对比剂后进行多时相重复扫描获得相应动态图像的检查方法,检查时间短、分辨率高。根据对比剂首次流经脑组织时引起的MR信号强度的变化,获得组织对比剂浓度—信号强度曲线,并计算出相关灌注参数,包括脑血流量(cerebral blood flow, CBF)、脑血容量(cerebral blood volume, CBV)、平均通过时间(mean transient time, MTT)、达峰时间(time to peak, TTP)及残余功能达峰时间(time to maximum of the residual function, Tmax)。目前指南和专家共识依据Tmax来决定组织窗,从而指导血管内治疗。相关研究[1, 2]定义缺血区为Tmax>6 s、梗死核心为ADC值<620×10-3 mm2/s的脑组织,缺血区与梗死核心区的不匹配区域为缺血半暗带。低灌注强度比值(hypoperfusion intensity ratio, HIR)由灌注成像获得,定义为Tmax>10 s与Tmax>6 s的组织体积比,低HIR可以提示良好侧支循环。Seners等[35]通过对具有大梗死核心的AIS-LVO患者研究发现PWI有助于选择可能从机械取栓治疗中受益的患者。Jiang等[36]对机械取栓治疗前后PWI参数的研究中发现MTT和TTP可能有助于预测治疗后早期再发梗死病灶的发生。Shin等[37]报道在接受机械取栓治疗前后的PWI各参数中,治疗后即刻TTP参数的恢复与良好预后及早期神经功能改善相关。尽管PWI需要注射外源性对比剂,有引起肾源性系统性纤维化的潜在风险,但是该技术在AIS评估中仍是临床常用的手段。

       ASL技术标记动脉血液中的水质子作为内源性示踪剂,反映了某一时刻脑血流量的大小及分布,通过测量CBF反映血流灌注的减低或增加。ASL根据标记方式的不同分为连续式动脉自旋标记(continuous arterial spin labeling, CASL)、脉冲式动脉自旋标记(pulsed arterial spin labeling, PASL)以及准连续式动脉自旋标记(pseudo-CASL, pCASL)。Liu等[38]研究证实ASL与DSC-PWI在识别缺血半暗带方面具有中~高度一致性。Lu等[39]研究发现对于机械取栓术后的AIS患者,术后ASL高灌注与血管成功再通相关,并可能为90 d神经功能恢复良好的独立预测指标。Thamm等[40]发现健侧大脑半球定量CBF是单侧大脑半球急性梗死患者90 d临床预后的重要预测因子。ASL还可以准确评估侧支循环[41, 42],当标记血液到达组织的时间长于标记后延迟时,延迟血流流速缓慢在ASL图像上表现为高信号,这些高信号被定义为动脉穿行伪影(artery transmit artifact, ATA)或动脉内高信号(intra-arterial high-intensity signal, IAS)。ATA位于皮质代表动脉闭塞导致的软脑膜侧支循环,IAS发生在近端代表动脉闭塞血流停滞,两个征象对于评价侧支循环及明确闭塞部位有重要意义[43]。Nam等[43]发现多时相ASL显示灌注受损与AIS患者早期复发性缺血病变(early recurrent ischemic lesions, ERLIs)的发生呈显著相关,当伴发ATA时这种相关性减弱而伴发IAS增强时,表明ASL相关参数可能有助于识别急性期发生ERLIs的高危患者。Mccullough-Hicks等[44]报道ASL上明亮血管征(bright vessel sign, BVS)诊断LVO较梯度回波序列(gradient echo, GRE)SVS征更敏感,然而仍需进一步研究证实其诊断价值。综上,ASL可定量评估侧支循环、缺血半暗带、脑灌注情况及确定血管闭塞部位,同时有一定的预后预测价值,在特定情况下可以作为DSC-PWI的替代检查方法。

6 酰胺质子转移成像

       酰胺质子转移(amide proton transfer, APT)成像技术是一种基于化学交换饱和转移(chemical exchange saturation transfer, CEST)原理的分子影像新技术,可以无创性反映被检组织的pH值和游离酰胺质子浓度。Cheung等[45]提出APT技术可以将PWI/DWI不匹配区细分为基于酸中毒的缺血半暗带(灌注和pH值均减低)和良性低灌注区(灌注减低,pH值正常)。Song等[46]研究发现APT技术可以反映AIS不同病理生理阶段,APT加权(APT weighted, APTw)信号强度随发病时间的延长而升高,同时APTw信号异质性(APTwmax-min)随发病时间的延长而减小。Yu等[47]通过随访观察临床常规支持治疗的AIS患者APTw信号变化,发现治疗有效的患者APTw信号强度显著升高而症状加重的患者则降低,表明APTw信号可以作为评估AIS治疗效果的影像标记物。Lin等[48]研究发现∆APTw(缺血区APTw信号与对侧正常脑组织APTw信号相对值)与NIHSS评分及mRS评分具有良好相关性,预后不良组的APTwipsi(缺血区)和∆APTw信号均显著低于预后良好组,预后不良组APTwmax-min明显高于预后良好组,表明定量分析APTw参数可以用来评估AIS患者病情程度及预测预后;此外梗死区域APTw信号的异质性(APTwmax-min)也可以作为判断临床预后的影像标记物。Momosaka等[49]研究不同预后的两组患者发现预后不良组APTw信号低于预后良好组,伴有大面积梗死且梗死区ADC值低、NIHSS及mRS评分高的患者APTw信号低,与Lin等[48]研究结果一致。多项研究[46, 47, 49]表明梗死区APT信号随发病时间的延长而增高,原因为梗死区组织pH值逐渐升高。然而,人体组织环境的异质性对于准确量化APT信号来说是一项难关,其会受到传统磁化转移效应以及核奥氏效应(nuclear overhauser effet, NOE)等影响。近年已有研究[50, 51]通过比较不同成像参数及量化方法以寻求最佳诊断标准。但是,APT检查技术受MRI设备及检查时间等限制,尚未在临床常规开展。

7 小结与展望

       MRI组织分辨率高,对AIS的诊断具有超高敏感性和特异性,在临床工作中得到认可并广泛开展。多模态MRI通过常规序列联合特殊序列反映缺血脑组织病理生理变化,不仅局限于诊断,还可以提示侧支循环、血流动力学、分子代谢等信息,为患者治疗方式的选择、疗效和预后的评估提供强有力的影像证据。多模态MRI临床应用价值巨大,但同时面临着序列选择及检查时间相对较长的问题。选择合适的技术取决于检查目的及实用性,因此如何制订最佳的检查方案依旧存在挑战。未来随着MRI技术的进步、新型程序的开发、人工智能技术以及深度学习技术的应用,会有更优方案以在最短检查时间内对AIS患者完成检查,同时迅速对大量图像数据进行分析以精确评估患者病情。

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