張雪鳳，劉崎，陳士躍，詹茜，彭雯佳，陳錄廣，田霞，陸建平

復(fù)發(fā)急性缺血性腦卒中患者大腦中動(dòng)脈斑塊的高分辨率MRI研究

張雪鳳，劉崎，陳士躍，詹茜，彭雯佳，陳錄廣，田霞，陸建平*

目的利用3.0 T高分辨磁共振(HR-MRI)研究復(fù)發(fā)急性缺血性腦卒中患者大腦中動(dòng)脈斑塊形態(tài)特征。材料與方法回顧性分析77例責(zé)任血管為大腦中動(dòng)脈的急性缺血性腦卒中患者資料，其中初發(fā)患者36例(初發(fā)組)，復(fù)發(fā)患者41例(復(fù)發(fā)組)，所有患者均行3.0 T高分辨磁共振斑塊成像(掃描序列包括TOF-MRA，頭顱常規(guī)DWI，責(zé)任血管軸位T1WI、T2WI及T1WIGd-DTPA增強(qiáng))。對(duì)比分析初發(fā)組與復(fù)發(fā)組急性缺血性腦卒中患者責(zé)任血管管腔狹窄率、最小管腔面積、斑塊負(fù)荷、斑塊強(qiáng)化率、T1WI及T2WI斑塊信號(hào)強(qiáng)度指數(shù)。結(jié)果復(fù)發(fā)組患者大腦中動(dòng)脈管腔狹窄率(P=0.002)、斑塊負(fù)荷(P=0.005)、斑塊強(qiáng)化率(P=0.037)均明顯高于初發(fā)組，最小管腔面積(P=0.001)明顯小于初發(fā)組。復(fù)發(fā)組斑塊T2WI信號(hào)強(qiáng)度指數(shù)大于初發(fā)組(P＜0.001)，而T1WI信號(hào)強(qiáng)度指數(shù)兩者無(wú)明顯差異(P=0.245)。結(jié)論高分辨率磁共振可以有效評(píng)估復(fù)發(fā)急性缺血性腦卒中患者大腦中動(dòng)脈斑塊的形態(tài)特征，綜合評(píng)價(jià)斑塊特征可為臨床提供參考以助于預(yù)防腦卒中復(fù)發(fā)。

梗塞，大腦中動(dòng)脈；磁共振成像；斑塊，動(dòng)脈粥樣硬化；復(fù)發(fā)

顱內(nèi)動(dòng)脈粥樣硬化是導(dǎo)致缺血性腦卒中的重要原因，在亞洲人口中這一比例約為33%～67%[1]，并以發(fā)生于大腦中動(dòng)脈的粥樣硬化病變?yōu)橹鳌Ｈ毖阅X卒中具有致死、致殘、復(fù)發(fā)率高的特點(diǎn)，并且每次復(fù)發(fā)造成的功能損害及疾病負(fù)擔(dān)均明顯大于首次發(fā)作，因此防治腦卒中復(fù)發(fā)意義重大。高分辨率磁共振(high-resolution magnetic resonance imaging，HR-MRI)可以用于評(píng)價(jià)斑塊易損性、預(yù)測(cè)急性腦卒中風(fēng)險(xiǎn)、判斷腦卒中預(yù)后[2-3]，但是目前尚缺乏復(fù)發(fā)腦卒中患者大腦中動(dòng)脈斑塊特征的研究報(bào)道。因此，筆者運(yùn)用HRMRI管壁成像技術(shù)定性、定量分析初發(fā)與復(fù)發(fā)大腦中動(dòng)脈斑塊形態(tài)學(xué)特征差異，旨在探討與復(fù)發(fā)急性缺血性腦卒中相關(guān)的大腦中動(dòng)脈斑塊形態(tài)特征，為預(yù)測(cè)腦卒中復(fù)發(fā)風(fēng)險(xiǎn)提供參考。

1 材料與方法

1.1 一般資料

收集2012年2月至2016年4月在上海長(zhǎng)海醫(yī)院因急性缺血性腦卒中在腦外科及神經(jīng)內(nèi)科住院患者資料，納入標(biāo)準(zhǔn)：(1)頭顱CTA、MRA或DSA顯示大腦中動(dòng)脈M1段狹窄；(2)有明確與狹窄側(cè)大腦中動(dòng)脈缺血性腦卒中相關(guān)的癥狀及體征，包括短暫性腦缺血發(fā)作；(3)發(fā)病1周內(nèi)行HR-MRI及常規(guī)頭顱DWI掃描；(4)具有頸部血管影像學(xué)檢查及心臟檢查資料。根據(jù)既往有無(wú)缺血性腦卒中發(fā)作分為初發(fā)組、復(fù)發(fā)組。初發(fā)組：缺血性腦卒中為首次發(fā)作。復(fù)發(fā)組：患者缺血性腦卒中原神經(jīng)系統(tǒng)癥狀和體征好轉(zhuǎn)和消失后，再次出現(xiàn)同側(cè)新的缺血癥狀及體征，或頭顱DWI發(fā)現(xiàn)同側(cè)新的梗死灶。排除標(biāo)準(zhǔn)：(1)同時(shí)存在同側(cè)顱內(nèi)動(dòng)脈或頸動(dòng)脈狹窄大于50%；(2)非動(dòng)脈粥樣硬化性顱內(nèi)動(dòng)脈狹窄，如合并心源性栓子、房顫、血管動(dòng)脈炎，動(dòng)脈夾層、高凝狀態(tài)等基礎(chǔ)疾?。?3)圖像質(zhì)量差無(wú)法診斷分析。所有患者均簽署知情同意書(shū)。

1.2 檢查方法

所有患者均在GE Signa HDxt 3.0 T磁共振設(shè)備上進(jìn)行檢查，依次進(jìn)行頭顱常規(guī)DWI、3D-TOF、HR-MRI序列掃描。DWI參數(shù)：TR 5300 ms，TE 74.3 ms，F(xiàn)OV 24 cm×24 cm，b=1000 s/mm2，激勵(lì)次數(shù)(NEX)2，矩陣160×160，層厚5 mm，掃描時(shí)間42 s。3D-TOF參數(shù)：TR 29 ms，TE 3.4 ms，F(xiàn)OV 24 cm×21.6 cm，激勵(lì)次數(shù)(NEX)為1，矩陣384×192，掃描時(shí)間4 min 47 s。根據(jù)3D-TOF圖像定位MCA走形區(qū)再行HR-MRI掃描，責(zé)任血管側(cè)大腦中動(dòng)脈掃描序列包括T2WI、T1WI、T1WIGd-DTPA增強(qiáng)，其中T2WI參數(shù)為：TR 2884 ms，TE 51 ms，F(xiàn)OV 10 cm×10 cm，NEX為6，矩陣320×256，回波鏈長(zhǎng)度(ETL)20，掃描時(shí)間3 min 51 s；T1WI參數(shù)為：TR 581 ms，TE 20 ms，F(xiàn)OV 10 cm×10 cm，NEX為4，矩陣320×256，ETL6，掃描時(shí)間5 min。高分辨率T1WI增強(qiáng)掃描采用Gd-DTPA對(duì)比劑，注射劑量0.2 mmol/kg，流率2 ml/s，注射對(duì)比劑后立即掃描。

1.3 圖像分析

掃描完成后將圖像導(dǎo)入PACS系統(tǒng)，由1名專(zhuān)門(mén)從事血管影像診斷的影像科醫(yī)師在不了解患者臨床資料的情況下進(jìn)行圖像分析。根據(jù)TOF-MRA測(cè)量大腦中動(dòng)脈最窄處管腔直徑和狹窄近端正常管腔直徑，根據(jù)WASID標(biāo)準(zhǔn)計(jì)算狹窄率[4]：狹窄率=(1-狹窄處直徑/狹窄近心端正常直徑)×100%。

根據(jù)HR-MRI圖像對(duì)大腦中動(dòng)脈斑塊進(jìn)行形態(tài)特征分析：包括最狹窄處管腔面積、斑塊負(fù)荷、斑塊T2WI及T1WI信號(hào)強(qiáng)度指數(shù)、斑塊強(qiáng)化率。利用CMRtools軟件(cardiovascular imaging solutions Ltd，UL)在T2WI圖像中手動(dòng)勾畫(huà)最狹窄處的管腔和管壁邊界，同時(shí)將此兩個(gè)血管輪廓拷貝至同層面T1WI及T1WI增強(qiáng)序列上。斑塊面積=管壁總面積-管腔面積；斑塊負(fù)荷=(斑塊面積/管壁總面積)×100%；斑塊(T1WI、T2WI、T1WI增強(qiáng))信號(hào)強(qiáng)度指數(shù)：斑塊平均信號(hào)強(qiáng)度/同層面灰質(zhì)信號(hào)強(qiáng)度；斑塊強(qiáng)化率=[(增強(qiáng)信號(hào)強(qiáng)度指數(shù)-平掃信號(hào)強(qiáng)度指數(shù))/平掃信號(hào)強(qiáng)度指數(shù)]×100%。

1.4 統(tǒng)計(jì)學(xué)分析

2 結(jié)果

本研究共納入77例患者，其中初發(fā)組36例，復(fù)發(fā)組41例，初發(fā)組男性31例(86.11%)，復(fù)發(fā)組男性25例(60.98%)，兩組男性患者比例均高于女性患者；初發(fā)組平均年齡(57.83±10.83)歲，復(fù)發(fā)組平均年齡(54.51±11.25)歲，兩者差異無(wú)統(tǒng)計(jì)學(xué)意義(P＞0.05)。

初發(fā)組與復(fù)發(fā)組責(zé)任側(cè)大腦中動(dòng)管腔狹窄率、斑塊負(fù)荷、斑塊強(qiáng)化率、最小管腔面積、T2WI及T1WI信號(hào)強(qiáng)度指數(shù)統(tǒng)計(jì)結(jié)果如表1所示。復(fù)發(fā)組患者大腦中動(dòng)脈管腔狹窄率(P=0.002)、斑塊負(fù)荷(P=0.005)、斑塊強(qiáng)化率(P=0.037)均明顯高于初發(fā)組患者，最小管腔面積(P=0.001)明顯小于初發(fā)組患者。復(fù)發(fā)組斑塊T2WI信號(hào)強(qiáng)度指數(shù)大于初發(fā)組(P＜0.001)，而T1WI信號(hào)強(qiáng)度指數(shù)無(wú)明顯差異(P=0.245)，圖1，2為1例復(fù)發(fā)組大腦中動(dòng)脈斑塊發(fā)病時(shí)及治療后HR-MRI表現(xiàn)。T1WI示復(fù)發(fā)組斑塊內(nèi)出血6例(14.63%)，初發(fā)組1例(2.78%)，兩者差別無(wú)統(tǒng)計(jì)學(xué)意義(χ2=1.986，P=0.113)。

3 討論

中國(guó)每年腦卒中新發(fā)病例約達(dá)250萬(wàn)，發(fā)病率和病死率居世界首位，其中70%為缺血性腦卒中[5]。缺血性腦卒中最主要原因?yàn)轱B內(nèi)動(dòng)脈粥樣硬化。癥狀性顱內(nèi)動(dòng)脈粥樣硬化有很高的臨床復(fù)發(fā)風(fēng)險(xiǎn)，風(fēng)險(xiǎn)高低因其狹窄部位而異，其中癥狀性大腦中動(dòng)脈狹窄患者，狹窄區(qū)域缺血性卒中的年復(fù)發(fā)率為7.8%[6]。Wang等[5]利用磁共振增強(qiáng)造影(MRA)研究了來(lái)自多中心2864例中國(guó)顱內(nèi)動(dòng)脈粥樣硬化患者臨床資料，結(jié)果顯示動(dòng)脈狹窄程度與腦卒中復(fù)發(fā)相關(guān)，狹窄程度越重越容易造成腦卒中復(fù)發(fā)。本研究發(fā)現(xiàn)復(fù)發(fā)組較初發(fā)組大腦中動(dòng)脈管腔狹窄率更高(P=0.002)，說(shuō)明血管狹窄程度越高復(fù)發(fā)風(fēng)險(xiǎn)越大，這與Wang等[5]的研究結(jié)果一致。但是動(dòng)脈粥樣硬化病變形成后是否導(dǎo)致臨床癥狀的出現(xiàn)，不僅取決于動(dòng)脈管腔的狹窄程度，與斑塊形態(tài)特征相關(guān)的斑塊穩(wěn)定性對(duì)臨床事件發(fā)生也起著重要的作用。本研究通過(guò)HR-MRI對(duì)比研究了初發(fā)與復(fù)發(fā)急性缺血性腦卒中患者大腦中動(dòng)脈斑塊形態(tài)特征差異，發(fā)現(xiàn)了除管腔狹窄程度外，復(fù)發(fā)性大腦中動(dòng)脈斑塊的一些高危特征。

本研究中復(fù)發(fā)組腦卒中患者斑塊負(fù)荷較初發(fā)組大(P=0.005)、最小管腔面積較初發(fā)組小(P=0.001)。彭雯佳等[7]在對(duì)大腦中動(dòng)脈粥樣硬化責(zé)任斑塊與非責(zé)任斑塊的形態(tài)學(xué)特征研究中，發(fā)現(xiàn)責(zé)任斑塊的斑塊負(fù)荷大于非責(zé)任斑塊并且最小管腔面積明顯小于非責(zé)任斑塊，對(duì)評(píng)估病變血管，斑塊負(fù)荷和最小管腔面積可作為管腔狹窄率的有益補(bǔ)充。另外在冠狀動(dòng)脈斑塊的研究中也發(fā)現(xiàn)了類(lèi)似的結(jié)果，研究發(fā)現(xiàn)冠脈的最小管腔面積≤4 mm2與急性心肌缺血癥狀相關(guān)，當(dāng)最小管腔面積≤4 mm2且斑塊負(fù)荷≥70%時(shí)則預(yù)測(cè)未來(lái)發(fā)生缺血事件的可能性大[8-9]。因此斑塊負(fù)荷大、最小管腔面積小，可作為評(píng)估復(fù)發(fā)腦卒中高危斑塊特征的重要參考。

本研究發(fā)現(xiàn)復(fù)發(fā)組斑塊的T2WI信號(hào)強(qiáng)度指數(shù)相對(duì)較高(P＜0.001)，Jiang等[10]在尸檢患者離體顱內(nèi)動(dòng)脈粥樣硬化斑塊的影像-病理對(duì)照研究中發(fā)現(xiàn)纖維帽或纖維組織的T2WI信號(hào)高，因此筆者認(rèn)為復(fù)發(fā)腦卒中高危斑塊可能含有較高比例的纖維帽或纖維組織成分。頸動(dòng)脈粥樣硬化斑塊組織學(xué)研究證實(shí)導(dǎo)致臨床事件的易損斑塊特征為斑塊內(nèi)出血、大的脂質(zhì)核心、薄的纖維帽、并伴有炎性細(xì)胞浸潤(rùn)[11]。T2WI高信號(hào)代表的纖維帽是高危斑塊的特征之一。斑塊內(nèi)出血T1WI表現(xiàn)為高信號(hào)，復(fù)發(fā)組斑塊內(nèi)出血比例高于初發(fā)組，但是兩者差異無(wú)統(tǒng)計(jì)學(xué)意義(P＞0.05)，T1WI信號(hào)強(qiáng)度指數(shù)在初發(fā)組與復(fù)發(fā)組亦無(wú)統(tǒng)計(jì)學(xué)差異(P＞0.05)。Xu等[12]在對(duì)急性缺血性腦卒中大腦中動(dòng)脈粥樣硬化斑塊的研究中認(rèn)為大腦中動(dòng)脈斑塊可能相對(duì)缺乏斑塊內(nèi)出血或血栓，本研究無(wú)論是初發(fā)組還是復(fù)發(fā)組急性缺血性腦卒中斑塊內(nèi)出血(T1WI高信號(hào))檢出比例均少，與這一結(jié)論相符。因此，根據(jù)T1WI信號(hào)強(qiáng)度指數(shù)尚不能評(píng)估復(fù)發(fā)斑塊風(fēng)險(xiǎn)。

表1初發(fā)組與復(fù)發(fā)組責(zé)任側(cè)大腦中動(dòng)脈管腔及斑塊形態(tài)學(xué)特征Tab. 1The morphological characteristics of the lumen and plaque of the culprit MCA in the primary group and the recurrent group

值得注意的是，本研究在T1WI增強(qiáng)序列上發(fā)現(xiàn)復(fù)發(fā)組斑塊的強(qiáng)化率較初發(fā)組高(P=0.037)，這提示斑塊強(qiáng)化率越高越有可能發(fā)生復(fù)發(fā)腦卒中事件。靜脈注射對(duì)比劑后斑塊的強(qiáng)化可反映斑塊內(nèi)新生血管、炎細(xì)胞浸潤(rùn)程度[13]。細(xì)胞內(nèi)微血管(新生血管)的形成一方面是供給斑塊營(yíng)養(yǎng)的來(lái)源，另一方面也是傳導(dǎo)、運(yùn)輸炎性細(xì)胞、炎性因子的渠道[14]。Moreno等[15]等發(fā)現(xiàn)新生血管和斑塊破裂有關(guān)，即與急性缺血事件密切相關(guān)。炎癥參與動(dòng)脈粥樣硬化的始動(dòng)環(huán)節(jié)與進(jìn)展過(guò)程。顱內(nèi)動(dòng)脈粥樣硬化斑塊的組織學(xué)研究發(fā)現(xiàn)，因顱內(nèi)血管炎癥抑制因子的減少、促炎水解酶的過(guò)度表達(dá)和外彈力層的缺失，顱內(nèi)動(dòng)脈粥樣硬化可能更容易受炎癥反應(yīng)的影響并且發(fā)生斑塊的失穩(wěn)[16]。因此，斑塊強(qiáng)化程度越高，提示腦卒中復(fù)發(fā)的風(fēng)險(xiǎn)越高。

本研究存在的不足：(1)本研究為回顧性研究、樣本量小，研究對(duì)象均為復(fù)發(fā)患者，缺少無(wú)復(fù)發(fā)缺血腦卒中患者對(duì)比分析，需要前瞻性、大樣本研究評(píng)估斑塊影像學(xué)特征對(duì)復(fù)發(fā)腦卒中風(fēng)險(xiǎn)的預(yù)判價(jià)值；(2)HR-MRI管壁成像掃描時(shí)間長(zhǎng)，本研究對(duì)象多為腦卒中癥狀相對(duì)較輕者，高齡、病情重、無(wú)法配合檢查者因不能行HR-MRI檢查而未選入研究中，如何縮短掃描時(shí)間、優(yōu)化成像序列使HR-MRI更全面的應(yīng)用于腦卒中患者是研究斑塊特征的關(guān)鍵。

圖1A～E圖為1例復(fù)發(fā)組患者的MRI圖像。TOF-MRA顯示右側(cè)大腦中動(dòng)脈M1段近端管腔狹窄90% (A)，DWI顯示右側(cè)側(cè)腦室旁新鮮腦梗死灶(B)；C～E圖為HR-MRI顯示大腦中動(dòng)脈管腔內(nèi)斑塊特征(箭頭)，T2WI斑塊高信號(hào)(C)，T1WI平掃斑塊等信號(hào)(D)，T1WI增強(qiáng)斑塊明顯強(qiáng)化(E)圖2為圖1同一患者經(jīng)抗凝、降脂治療3個(gè)月后復(fù)查圖像，期間未出現(xiàn)復(fù)發(fā)腦卒中。TOF顯示右側(cè)大腦中動(dòng)脈M1段近端狹窄程度明顯改善(A)，DWI示右側(cè)腦室旁陳舊腦梗死灶(B；箭頭)，T2WI示斑塊變小、信號(hào)減低(C)，T1WI增強(qiáng)斑塊強(qiáng)化程度明顯減低(D)Fig. 1A—E images are MRI images in the same patient of recurrent group, TOF-MRA shows right middle cerebral artery M1 segment proximal 90% stenosis (A), DWI shows right lateral ventricle fresh cerebral infarction (B). C—E images are HR-MRI shows the middle cerebral artery plaque (arrow), T2WI shows high signal of the plaque (C), T1WI shows equal signal of the plaque (D), contrast-enhanced T1WI shows obvious enhancement of plaque (E).Fig. 2A—D images are MRI images in the same patient of Fig.1 after anticoagulation, lipid lowering treatment for three months, there was no recurrence stroke during the period. TOF shows the degree of stenosis signif i cantly improved (A), DWI shows old cerebral infarction (B, arrow), the area and T2WI signal intensity of plaque was reduced (C), plaque enhancement decreased signif i cantly (D).2D

綜上所述，高分辨率MRI可以有效評(píng)估復(fù)發(fā)急性缺血性腦卒中患者大腦中動(dòng)脈斑塊形態(tài)特征；復(fù)發(fā)大腦中動(dòng)脈管腔狹窄程度更重、斑塊負(fù)荷更大、最小管腔面積小、斑塊T2WI信號(hào)相對(duì)較高并且強(qiáng)化程度更明顯，綜合斑塊的這些特征，可早期識(shí)別易復(fù)發(fā)高危斑塊，更好地為臨床評(píng)估復(fù)發(fā)腦卒中風(fēng)險(xiǎn)提供參考，以減少缺血性腦卒中復(fù)發(fā)事件。

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Middle cerebral artery plaque in patients with recurrent acute ischemic stroke: studied with high-resolution magnetic resonance imaging

ZHANG Xue-feng, LIU Qi, CHEN Shi-yue, ZHAN Qian, PENG Wen-jia, CHEN Luguang, TIAN Xia, LU Jian-ping*
Department of Radiology, Changhai Hospital, the Second Military Medical University, Shanghai 200433, China

Objective:To study the morphological characteristics of middle cerebral artery plaque in patients with recurrent acute ischemic stroke by 3.0 T high resolution magnetic resonance imaging (HR-MRI).Materials and Methods:Retrospective analysis of clinical data of 77 cases of patients with acute ischemic stroke, the culprit plaques in middle cerebral artery, including 36 cases of patients with primary (primary group), 41 cases with recurrence (recurrence group), all patients underwent 3.0 T high resolution magnetic resonance imaging (plaque scanning sequence including TOF-MRA, DWI for the whole brain, T1WI,T2WI and contrast-enhanced T1WI). Comparative analysis of the primary and recurrent patients plaque morphological characteristics included lumen stenosis rate, minimal lumen area, plaque burden, plaque enhancement rate, T1WI and T2WI plaque signal strength index.Results:The lumen stenosis rate (P=0.002), plaque burden (P=0.005) and plaque enhancement ratio (P=0.037) were signif i cantly higher in the recurrent group than in the primary group, and the minimal lumen area (P=0.001) was signif i cantly smaller than that in the primary group. The T2WI signal intensity index of the recurrence group was higher than that of the primary group (P＜0.001), while the T1WI signal strength index was not signif i cantly different (P=0.245).Conclusions:High resolution magnetic resonance imaging can effectively evaluate the morphological characteristics of middle cerebral artery plaque in patients with recurrent acute ischemic stroke. Comprehensiveevaluation of plaque characteristics can provide reference for the clinical and help to prevent recurrence stroke.

Infarction, middle cerebral artery; Magnetic resonance imaging; Plaque, atherosclerotic; Recurrence

國(guó)家自然科學(xué)基金面上項(xiàng)目(編號(hào)：31470910)；上海市市級(jí)醫(yī)院新興前沿技術(shù)聯(lián)合攻關(guān)項(xiàng)目(編號(hào)：SHDC12013110)；全軍醫(yī)學(xué)科研“十二五”計(jì)劃重點(diǎn)課題(編號(hào)BWS12J026)

第二軍醫(yī)大學(xué)附屬長(zhǎng)海醫(yī)院影像醫(yī)學(xué)科，上海 200433

陸建平，E-mail：cjr.lujianping@ vip.163.com

2016-09-23

接受日期：2016-10-13

R445.2；R743.33

A

10.12015/issn.1674-8034.2016.11.003

張雪鳳, 劉崎, 陳士躍, 等. 復(fù)發(fā)急性缺血性腦卒中患者大腦中動(dòng)脈斑塊的高分辨率MRI研究. 磁共振成像, 2016, 7(11): 808-812.

*Correspondence to: Lu JP, E-mail: cjr.lujianping@vip.163.com

Received 23 Sep 2016, Accepted 13 Oct 2016

ACKNOWLEDGMENTSThe National Nature Science Foundation of China (No. 31470910). The Emerging Frontier Technology Joint Research Program of Shanghai Municipal Hospital, China (No. SHDC12013110). The twelth f i ve-year plan of medical key project of the People's Liberation Army (No. BWS12J026).