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临床研究
症状性大脑中动脉粥样硬化狭窄患者DWI与HRMR-VWI特征分析:青年与中老年组的比较
吕霞 赵家欣 马泽兰 刘岘 刘国清

Cite this article as: Lü X, Zhao JX, Ma ZL, et al. Characteristic analysis of DWI and HRMR-VWI in patients with symptomatic middle cerebral atherosclerotic stenosis: comparison between the young group and middle-aged and elderly group[J]. Chin J Magn Reson Imaging, 2022, 13(1): 1-5, 10.本文引用格式:吕霞, 赵家欣, 马泽兰, 等. 症状性大脑中动脉粥样硬化狭窄患者DWI与HRMR-VWI特征分析:青年与中老年组的比较[J]. 磁共振成像, 2022, 13(1): 1-5, 10. DOI:10.12015/issn.1674-8034.2022.01.001.


[摘要] 目的 基于扩散加权成像(diffusion weighted imaging,DWI)及高分辨磁共振血管壁成像(high resolution magnetic resonance vessel wall imaging,HRMR-VWI)探讨不同年龄段症状性大脑中动脉粥样硬化性狭窄(symptomatic middle cerebral atherosclerotic stenosis,sMCAS)患者在卒中机制及责任血管管壁特征的差异。材料与方法 连续纳入2019年8月至2021年4月因sMCAS导致缺血性卒中或短暂性缺血发作的患者,根据年龄分为青年组(≤45岁)和中老年组(>45岁)。根据DWI急性脑梗死灶的分布模式判定sMCAS卒中机制,包括穿支动脉受累组、低灌注组、动脉-动脉栓塞组及多种机制组。分析两组患者在危险因素方面和卒中机制的差异,以及责任血管在HRMR-VWI管壁特征的差异,包括斑块面积、负荷、长度、强化模式、斑块内出血、斑块分布模式及责任血管的狭窄率、重构指数、重构模式。结果 纳入sMCAS患者103例,其中青年患者30例,中老年患者73例,两组患者在高血压和冠心病方面差异有统计学意义(P<0.05);青年组和中老年组的卒中机制差异无统计学意义(P>0.05)。两组患者责任血管在HRMR-VWI管壁特征的比较:中老年组的斑块面积、斑块负荷及血管重构指数均大于青年组,差异有统计学意义(P<0.05);两组患者在斑块长度、斑块强化模式、斑块内出血、斑块分布及血管狭窄率、重构模式上差异无统计学意义(P>0.05)。结论 青年组和中老年组sMCAS患者在斑块面积、斑块负荷及血管重构指数存在差异,提示青年sMCAS的病理生理学改变有所不同,其干预策略可能有别于中老年患者。
[Abstract] Objective To investigate the differences of the characteristics of responsible vessel wall between young and middle-aged and elderly patients with symptomatic middle cerebral atherosclerotic stenosis (sMCAS) based on high resolution magnetic resonance vessel wall imaging (HRMR-VWI).Materials and Methods: From August 2019 to April 2021,consecutive patients with ischemic stroke or transient ischemic attack caused by sMCAS were selected and divided into young group (≤45 years old) and middle-aged and elderly group (>45 years old). The mechanism of sMCAS stroke was determined according to the distribution pattern of acute cerebral infarction on DWI, including parent artery occluding penetrating artery, hypoperfusion, artery-artery embolization and multiple mechanism. The differences of risk factors between the two groups and the differences of HRMR-VWI wall characteristics of responsible vessels were analyzed, including plaque area, plaque burden, length, enhancement pattern, intraplaque bleeding, plaque distribution pattern, stenosis rate of responsible vessels, remodeling index and remodeling pattern.Results One hundred and three patients with sMCAS were included, including 30 young patients and 73 middle-aged and elderly patients. There were significant differences in hypertension and coronary heart disease between the two groups (P<0.05); there was no significant difference in the mechanism of sMCAS stroke between the two groups (P>0.05).The plaque area, plaque burden and vascular remodeling index of the middle-aged and elderly group were higher than those of the young group (P<0.05); there was no significant difference in plaque length, plaque enhancement pattern, intraplaque bleeding, plaque distribution, stenosis rate and remodeling pattern between the two groups (P>0.05).Conclusions There are differences in plaque area, plaque burden and vascular remodeling index between young and middle aged-elderly patients with sMCAS, suggesting that the pathophysiological changes of young patients with sMCAS are different, and their intervention strategies may be different from those of middle-aged and elderly patients.
[关键词] 扩散加权成像;高分辨磁共振血管壁成像;大脑中动脉;动脉粥样硬化;年龄
[Keywords] diffusion weighted imaging;high resolution magnetic resonance vessel wall imaging;middle cerebral artery;atherosclerosis;age

吕霞    赵家欣    马泽兰 *   刘岘    刘国清   

广东省中医院影像科,广州 510120

马泽兰,E-mail:305131863@qq.com

全部作者均声明无利益冲突。


基金项目: 国家自然科学基金 81801688
收稿日期:2021-07-16
接受日期:2021-11-10
中图分类号:R445.2  R541.4 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2022.01.001
本文引用格式:吕霞, 赵家欣, 马泽兰, 等. 症状性大脑中动脉粥样硬化狭窄患者DWI与HRMR-VWI特征分析:青年与中老年组的比较[J]. 磁共振成像, 2022, 13(1): 1-5, 10. DOI:10.12015/issn.1674-8034.2022.01.001

       近年来,我国青年缺血性脑卒中的发病率逐年增高,其主要病因是症状性大脑中动脉粥样硬化性狭窄(symptomatic middle cerebral atherosclerotic stenosis,sMCAS),该病因所致的脑卒中复发风险高,严重威胁国民健康[1, 2]。然而,目前针对青年sMCAS患者的研究极少,不同年龄段sMCAS患者脑卒中机制和责任动脉管壁改变是否存在差异尚不清楚,青年卒中的诊治方案主要参考基于中老年人为主的研究结果。近期有研究[3, 4]发现大脑中动脉的斑块负荷、重构方式与年龄存在相关性,但这些研究并非针对症状性粥样硬化性狭窄患者,且仅对病变管壁的形态特征进行评估,无涉及斑块的成分评估,存在较大的局限性。高分辨磁共振血管壁成像(high resolution magnetic resonance vessel wall imaging,HRMR-VWI)作为当前唯一可用于无创评估颅内动脉管壁结构分析的技术,具有非常重要的临床应用价值[5]。本研究拟利用扩散加权成像(diffusion weighted imaging,DWI)及HRMR-VWI对青年与中老年sMCAS患者急性脑梗死灶分布模式及责任血管管壁特征进行比较,探讨两组年龄段患者在卒中机制及血管病理改变的差异,为临床个体化卒中预防与治疗提供支持证据。

1 材料与方法

1.1 研究对象

       本研究经过广东省中医院伦理委员会批准(批准文号:BE2019-180-01),免除受试者知情同意。本研究回顾性连续纳入我院2019年8月至2021年4月期间103例sMCAS患者病例作为研究对象。根据2017年发表的《症状性颅内外动脉粥样硬化性大动脉狭窄管理规范—中国卒中学会科学声明》,本研究中sMCAS定义为就诊两周内发生缺血性卒中和(或)短暂性脑缺血发作,影像学发现大脑中动脉粥样硬化性狭窄,狭窄程度为50%~99%,且梗死灶位于大脑中动脉供血区或者短暂性脑缺血发作症状与大脑中动脉供血区神经功能相匹配[6]。根据年龄将sMCAS患者分为青年组(≤45岁)和中老年组(>45岁)[7],记录所有患者临床资料,包括:性别、年龄、高血压、高血脂、糖尿病、吸烟、卒中或短暂性脑缺血发作(transient ischemic attack,TIA)病史、冠心病、体质量指数(Body Mass Index,BMI)以及入院时美国国立卫生研究院卒中量表(National Institute of Health Stroke Scale,NIHSS)评分。

       纳入标准:(1)均行HRMR-VWI检查,且在该检查前/后3天内均进行了DWI及磁共振血管成像(magnetic resonance angiograph,MRA)扫描,上述图像质量良好;(2)大脑中动脉局限性狭窄位于M1段,且狭窄程度为50%~99%。排除标准:(1)存在心源性卒中及其他可能病因,如血管炎、凝血异常等;(2)同侧颈总动脉或颈内动脉狭窄并存患者(狭窄>50%)。最终,本研究纳入sMCAS患者103例,其中青年患者30例,中老年患者73例。

1.2 影像学检查

       采用3.0 T西门子MR扫描仪(MAGNETOM Prisma, Siemens Healthineers),64通道头颈联合线圈。HRMR-VMI扫描采用三维可变翻转角度快速自旋回波(sampling perfection with application of optimized contrasts using different flip angle evolution,SPACE) T1WI序列,矢状位覆盖头颅范围,参数如下:TR 800 ms,TE 19 ms,FOV 207 mm×178 mm,层厚 0.54 mm,层数256,矩阵 330×384。使用高压注射器注射对比剂5 min后进行重复扫描,对比剂为钆喷酸葡胺,注射剂量为0.2 mL/kg。DWI参数:TR 4040 ms,TE 91 ms,FOV 220 mm×220 mm,b=1000 s/mm2,激励次数2,矩阵160×160,层厚5 mm;MRA参数:TR 21 ms,TE 3.42 ms,FOV 200 mm×200 mm,激励次数1,矩阵319×384。

1.3 图像后处理及分析方法

       把原始数据导入后处理工作站,由两名有经验的影像科医生在工作站上采用盲法独立分析急性脑梗死的分布模式和责任血管的HRMR-VWI影像学特征,意见不一致时咨询第三位更有经验的放射科医师,做出最终决定。根据DWI急性脑梗死灶的分布模式判定卒中机制,分为:(1)穿支动脉受累组:梗死灶位于sMCAS部位的穿支动脉供血区;(2)低灌注组:梗死灶位于两条血管交界区;(3)动脉-动脉栓塞组:梗死灶位于大脑中动脉支配区域内的多发性梗死或皮层单发梗死;(4)多种机制组:存在2个或2个以上的上述卒中机制。分析责任血管的HRMR-VWI影像学特征包括斑块面积、斑块负荷、斑块长度、强化模式、斑块内出血、斑块分布模式及相应血管的狭窄率、重构指数、重构模式。选择病变血管最狭窄处的层面(maximal lumen narrowing,MLN)作为测量层面,取(病变近心端正常层面+远心端正常层面)/2的数值为参考层面(referential lumen,RL),在上述层面勾画血管管腔轮廓及血管壁轮廓,分别得到相应的血管面积(vessel area,VA)和管腔面积(1umen area,LA),测量参数公式如下[8]:狭窄率=(1-LAMLN/LARL)×100%;管壁面积(Wall area,WA)=VA-LA,斑块面积=WAMLN-WARL;斑块负荷=(WAMLN-WARL)/VA×100%;重构指数(remodeling index,RI)=VAMLN/VARL。重构模式:重构指数>1.05为正性重构,重构指数<0.95为负性重构,重构指数在0.95~1.05为无明显重构,将后两者归为非正性重构[9]。斑块强化模式以正常管壁为参考,斑块强化程度低于或等于正常管壁为无强化组,斑块强化程度高于正常管壁为有强化组[10]。斑块内出血指T1WI平扫图像上斑块信号强度大于附近脑灰质信号强度150%[11]。斑块分布模式分为环形斑块和偏心性斑块,通过多平面重建,取病变大脑中动脉最狭窄处的正交界面,以管腔中心点及水平线为基准作两条与水平线45°角斜线,血管被划分为4个象限:腹侧、背侧、上、下共四个象限,若斑块覆盖范围累及1或2个象限为偏心性斑块,累及3或4个象限为环形斑块[12]

1.4 统计学分析

       应用SPSS 22.0统计软件进行分析。对于计量资料,采用Kolmogorov-Smirnov检验进行正态性检验,以Levene检验对其进行方差齐性检验,符合正态分布的变量采用x¯±s表示,不符合正态分布的变量采用中位数(四分位间距)表示,以独立样本t检验(符合正态分布及方差齐性假设)或Mann-Whitney U检验(不符合正态分布或方差齐性假设)检验两组患者间的不同变量的差异。对于计数资料,采用卡方检验或Fisher's确切检验法比较两组患者间的差异。P<0.05认为差异有统计学意义。

2 结果

2.1 一般临床资料

       103例患者纳入分析,其中青年患者30例,平均年龄40.5岁,中老年患者73例,平均年龄62岁。两组患者在年龄(P<0.001)、高血压(t=21.208,P<0.001)和冠心病(t=4.053,P=0.044)方面差异有统计学意义,而在性别、高血脂、糖尿病、吸烟、卒中或TIA病史、BMI、入院NIHSS评分上,两组间差异无统计学意义(P>0.05),见表1

表1  青年组与中老年sMCAS患者一般资料的比较
Tab. 1  Comparison of general data between the young group and middle-aged and elderly group

2.2 青年和中老年sMCAS患者卒中机制的比较

       青年组和中老年组分别有22例和53例患者表现为缺血性卒中,青年组以穿支动脉受累型最常见,次之为动脉-动脉栓塞型,而中老年组以多种机制型最常见,次之为穿支动脉受累型。然而,两组患者在四种卒中机制方面差异均无统计学意义(P>0.05),见表2

表2  青年和中老年sMCAS患者卒中机制的比较
Tab. 2  Comparison of mechanisms of stroke between the young group and middle-aged and elderly group

2.3 青年和中老年sMCAS患者责任血管HRMR-VWI特征比较

       青年组与中老年组sMCAS患者在斑块面积[(中位数1.85,四分位间距2.71) vs. (中位数3.35,四分位间距2.81),P=0.026]、斑块负荷[(中位数21.58,四分位间距22.13) vs. (中位数31.13,四分位间距20.48),P=0.008]及血管重构指数[(1.08±0.16) vs. (1.00±0.16),P=0.032)]方面差异有统计学意义,以上指标老年组均高于青年组,见图12。两组患者在斑块长度、斑块强化模式、斑块分布模式、斑块内出血发生率、血管狭窄率及重构模式方面差异均无统计学意义(P>0.05),见表3

图1  女,43岁,右侧大脑中动脉图像。A:MRA示右侧大脑中动脉M1段重度狭窄(线条1、2、3分别代表图B、C、D所在的层面);B~D:T1WI增强扫描矢状位图。右侧大脑中动脉的近端正常参考层面(B)、管腔最狭窄层面(C)和远端正常参考层面(D)及相应的放大图。B图示近端正常参考层面的血管面积为7.35 mm2,管腔面积为2.98 mm2;C图示管腔最狭窄层面的血管面积为6.52 mm2,管腔面积为0.74 mm2;D图示远端正常参考层面的血管面积为6.64 mm2,管腔面积为2.34 mm2。病变血管狭窄率为72.18%,斑块面积为1.445 mm2,斑块负荷为22.16%,重构指数为0.93 (负性重构)。
Fig. 1  Images of the right middle cerebral artery in a 43-year-old woman. A: MRA shows severe stenosis in the M1 segment of right middle cerebral artery (Lines 1, 2, and 3 represent the sites of figure B, C, and D, respectively). B-D:Sagittal view of post-contrast T1-weighted images. The proximal reference site (B), the maximal-lumen-narrowing site (C) and the distal reference site (D) of right middle cerebral artery are shown. The vessel area or lumen area are 7.35 mm2 and 2.98 mm2 in the proximal reference site (B),6.52 mm2 and 0.74 mm2 in the maximal-lumen-narrowing site (C) and 6.64 mm2 and 2.34 mm2 in the distal reference site (D). The degree of stenosis is 72.18%, the plaque area is 1.445 mm2, and percentage of plaque burden is 22.16%. The remodeling index is 0.93 (defined as negative remodeling).
图2  女,67岁,右侧大脑中动脉图像。A:MRA示右侧大脑中动脉M1段重度狭窄(线条1、2、3分别代表图B、C、D所在的层面);B~D:T1WI增强扫描矢状位图。右侧大脑中动脉的近端正常参考层面(B)、管腔最狭窄层面(C)和远端正常参考层面(D)及相应的放大图。B图示近端正常参考层面的血管面积为7.93 mm2,管腔面积为3.24 mm2;C图示管腔最狭窄层面的血管面积为8.32 mm2,管腔面积为0.67 mm2;D图示远端正常参考层面的血管面积为7.07 mm2,管腔面积为2.84 mm2。病变血管狭窄率为77.85%,斑块面积为3.175 mm2,斑块负荷为38.16%,重构指数为1.11 (正性重构)。
Fig. 2  Images of the right middle cerebral artery in a 67-year-old woman. A: MRA shows severe stenosis in the M1 segment of right middle cerebral artery (Lines 1, 2, and 3 represent the sites of figure B, C, and D, respectively). B-D:Sagittal view of post-contrast T1-weighted images. The proximal reference site (B), the maximal-lumen-narrowing site (C) and the distal reference site (D) of right middle cerebral artery are shown. The vessel area or lumen area are 7.93 mm2 and 3.24 mm2 in the proximal reference site (B),8.32 mm2 and 0.67 mm2 in the maximal-lumen-narrowing site (C) and 7.07 mm2 and 2.84 mm2 in the distal reference site (D). The degree of stenosis is 77.85%, the plaque area is 3.175 mm2, and percentage of plaque burden is 38.16%. The remodeling index is 1.11 (defined as positive remodeling).
表3  青年和中老年sMCAS患者责任血管HRMR-VWI特征比较
Tab. 3  Comparison of the characteristics of responsible vessel wall on HRMR-VWI between the young group and middle-aged and elderly group

3 讨论

       本研究基于DWI与HRMR-VWI技术评估青年组sMCAS患者与中老年组sMCAS患者的致卒中机制及责任血管管壁的影像学特征,研究结果显示中老年组的斑块面积、斑块负荷及血管重构指数均明显大于青年组,而在卒中机制方面,两组患者差异无统计学意义。本研究首次联合DWI与HRMR-VWI两种无创技术对不同年龄段sMCAS患者进行影像学特征比较,有助于理解不同年龄段sMCAS患者潜在的病理生理发展机制,为缺血性脑卒中的个体化防治提供更多的依据。

3.1 责任血管HRMR-VWI特征

       由于大脑中动脉M1段是症状性颅内动脉粥样硬化性狭窄最好发的部位,且该段血管较为平直,在形态学测量方面可以达到较高的准确度,因此本研究选取该部位的病变作为研究对象。血管重构是血管壁对动脉粥样硬化的适应性改变,其病例生理机制尚未完全阐明。动脉重构主要分为动脉代偿性扩张即正性重构和动脉壁皱缩即负性重构[13]。本研究的中老年组正性重构比例为56.2%,与高佩红[3]等报道的中老年组正性重构比例为55.32%相近,在重构指数方面,中老年组明显高于青年组,提示年龄与动脉重构存在相关性,亦与既往研究结果相符[3, 4]。该现象可能与颅内动脉血管壁的组织学有关,随着年龄增长,血管弹力纤维的劳损和破坏会引起动脉壁扩张[14]。此外,斑块成分、斑块大小、斑块稳定性对血管重构也会发生影响,质地偏软、体积大、容易破裂的斑块更容易发生正性重构[15, 16],本研究中老年组斑块面积及负荷均大于青年组,可能是造成中老年组重构率较大的原因之一。另外,血流动力学状态、血管内皮功能对重构方式也有一定的影响[17, 18],但其与年龄的关系还有待进一步深入研究。

       本研究中老年组sMCAS患者斑块面积、斑块负荷均明显高于青年组,与既往学者[3, 4,19]的研究结果相一致。该现象可能由于随着年龄的增长,血管危险因素的发生率增高[20],如在本研究中,中老年高血压的患病率较青年人明显增高,而既往研究发现高血压可导致内皮细胞功能下降,动脉内膜下脂质沉积,平滑肌细胞增生和纤维基质成分增殖,从而加快动脉粥样硬化的发展进程21。另外,年龄的增长及多种病理因素的影响,导致颅内动脉滋养血管增多也可能是导致斑块进展的原因之一[22]

3.2 致卒中机制

       本研究结果与陈红兵等[20]的研究结果相似,即青年与中老年sMCAS患者在卒中机制方面差异无统计学意义。该结果可能与研究入选的sMCAS患者责任血管狭窄程度均为中度或重度狭窄有关,由于重度狭窄患者更容易发生低灌注,这将导致研究对象的致卒中机制存在重叠。因此,未来有必要针对不同狭窄程度的患者进行分组,独立观察两组患者在卒中机制方面的差异。

3.3 研究的局限性

       本研究存在以下不足:(1)单中心研究,样本量相对偏小,还需进行大样本、多中心研究进一步证实;(2)本研究只针对症状性粥样硬化患者,未来有必要纳入无症状组进行对照;(3)由于通常难以获得大脑中动脉的病理标本,对其斑块成分的评估未能与组织学相对应。

       综上所述,对于不同年龄段sMCAS患者的二级预防,由于中老年sMCAS患者高血压的患病率高于青年人,斑块面积、斑块负荷及血管重构指数均高于青年患者,临床医师需要特别重视sMCAS患者在卒中危险因素如高血压的早期管理,同时,相比青年患者,中老年患者在药物治疗上可能需要进一步强化,但这方面仍有待更多相关的研究加以验证。

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