應(yīng)用高分辨率磁共振成像評(píng)估腦動(dòng)脈粥樣硬化斑塊的研究進(jìn)展①

于瑾，白皛，吳士文，徐蔚海，吳衛(wèi)平

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應(yīng)用高分辨率磁共振成像評(píng)估腦動(dòng)脈粥樣硬化斑塊的研究進(jìn)展①

于瑾1,2a，白皛2b，吳士文2a，徐蔚海3，吳衛(wèi)平1

[摘要]高分辨率磁共振成像(HRMRI)是一項(xiàng)安全、無創(chuàng)、經(jīng)濟(jì)和可重復(fù)的檢查方法，可以精確反映動(dòng)脈粥樣硬化的程度，對(duì)未來的臨床事件有較高的預(yù)測(cè)價(jià)值。其核磁掃描像素可達(dá)到亞毫米級(jí)，采用“黑血”技術(shù)，廣泛應(yīng)用于動(dòng)脈管壁及斑塊成分的研究。應(yīng)用HRMRI評(píng)估腦動(dòng)脈粥樣硬化斑塊的易損性，包括動(dòng)脈重塑、斑塊負(fù)荷、斑塊內(nèi)出血和強(qiáng)化、斑塊分布等特點(diǎn)，具有重要的臨床意義。

[關(guān)鍵詞]高分辨率；磁共振成像；腦動(dòng)脈；動(dòng)脈粥樣硬化；斑塊；綜述

[本文著錄格式]于瑾，白皛，吳士文，等.應(yīng)用高分辨率磁共振成像評(píng)估腦動(dòng)脈粥樣硬化斑塊的研究進(jìn)展[J].中國(guó)康復(fù)理論與實(shí)踐, 2016, 22(2): 164-167.

CITED AS: Yu J, Bai X, Wu SW, et al. Progress of high-resolution magnetic resonance imaging in evaluating cerebral atherosclerotic plaques (review) [J]. Zhongguo Kangfu Lilun Yu Shijian, 2016, 22(2): 164-167.

作者單位：1.解放軍總醫(yī)院老年神經(jīng)內(nèi)科，北京市100853；2.武警總醫(yī)院，a.神經(jīng)內(nèi)科；b.南一科，北京市100039；3.中國(guó)醫(yī)學(xué)科學(xué)院北京協(xié)和醫(yī)院神經(jīng)科，北京市100730。作者簡(jiǎn)介：于瑾(1980-)，女，漢族，河北保定市人，醫(yī)學(xué)碩士，主治醫(yī)師，主要研究方向：顱內(nèi)動(dòng)脈的高分辨率磁共振研究。通訊作者：吳衛(wèi)平，男，醫(yī)學(xué)博士，主任醫(yī)師。E-mail: wuwp@vip.sina.com。

對(duì)于腦動(dòng)脈粥樣硬化性疾病，理想的成像方法應(yīng)該是安全、無創(chuàng)、經(jīng)濟(jì)和可重復(fù)的，并且可以精確反映動(dòng)脈粥樣硬化的程度，對(duì)未來的臨床事件有較高的預(yù)測(cè)價(jià)值。高分辨率磁共振成像(high-resolution MRI, HRMRI)能夠在常規(guī)血管影像檢查檢測(cè)到斑塊之前發(fā)現(xiàn)動(dòng)脈粥樣硬化斑塊，提供更敏感和更客觀的信息。它是一項(xiàng)符合上述要求，且最具潛力的影像技術(shù)。近年來HRMRI在臨床中得到廣泛應(yīng)用，發(fā)展迅速，已應(yīng)用于頸動(dòng)脈[1]、主動(dòng)脈[2]、外周動(dòng)脈[3-4]，冠狀動(dòng)脈[5]以及顱內(nèi)血管，包括大腦中動(dòng)脈[6]和基底動(dòng)脈[7]。本文對(duì)近年來應(yīng)用HRMRI評(píng)估腦動(dòng)脈粥樣硬化斑塊的研究予以綜述。

1　HRMRI的相關(guān)成像技術(shù)

用于血管成像的磁共振成像脈沖序列包括“亮血”和“黑血”技術(shù)。目前廣泛應(yīng)用的三維時(shí)間飛躍法磁共振血管造影(three-dimension time of flight magnetic resonance angiography, 3D TOF MRA)即“亮血”技術(shù)，此技術(shù)基于血液的流入增強(qiáng)效應(yīng)，采集時(shí)間短。然而此技術(shù)僅能評(píng)估管腔的狹窄率，隨著對(duì)管壁結(jié)構(gòu)和動(dòng)脈粥樣硬化斑塊成分的關(guān)注，研究人員對(duì)磁共振成像硬件和序列設(shè)計(jì)提出新的要求。

HRMRI是指核磁掃描像素達(dá)到亞毫米級(jí)，采用“黑血”技術(shù)，使用脈沖抑制血流信號(hào)，血流呈黑色低信號(hào)，而周圍組織為高信號(hào)，從而產(chǎn)生對(duì)比，襯托出管壁斑塊的影像。目前臨床上為了使管壁影像獲得充足的空間分辨率和對(duì)比，使用3 T 或7 T的核磁掃描機(jī)和專用的高頻線圈以獲得較高的信噪比(signal-to-noise ratio, SNR)、對(duì)比噪聲比(contrast-to-noise ratio, CNR)和信號(hào)穿透深度。動(dòng)脈粥樣硬化斑塊的成分依靠磁共振成像信號(hào)強(qiáng)弱進(jìn)行辨別，而多模式序列顯示斑塊成分更有意義[8]，包括2維T1加權(quán)圖像(T1weighted imaging, T1WI)，T2加權(quán)圖像(T2weighted imaging, T2WI)和質(zhì)子密度加權(quán)圖像(proton density weighted imaging, PDWI)。脂質(zhì)成分在T1WI、PDWI是高信號(hào)，在T2WI是低信號(hào)；纖維蛋白成分在3個(gè)序列都是高信號(hào)；鈣離子在3個(gè)序列都是低信號(hào)；血栓在3個(gè)序列也都是高信號(hào)，但比纖維蛋白的信號(hào)稍低[9]。T1WI易于觀察出血，但不能清楚地顯示外邊界。PDWI比T1WI及T2WI的圖像對(duì)比度高，可以更好地分辨管壁和管腔，而T1WI及T2WI圖像更有利于顯示斑塊的不均質(zhì)成分[1]。

3D HRMRI具有各向同性體素，可以通過減少部分容積效應(yīng)檢測(cè)細(xì)微的血管壁病變，同時(shí)可以更好地抑制腦脊髓液流進(jìn)行任何平面的自由重建。然而，3D影像的缺點(diǎn)是空間分辨率不如2D影像。

2　HRMRI在血管評(píng)估上的應(yīng)用進(jìn)展

1996年，Toussaint等最早提出MRI可以精確測(cè)量和分辨體內(nèi)的頸動(dòng)脈斑塊[10]。頸動(dòng)脈因其位置表淺，不易移動(dòng)，比主動(dòng)脈和冠狀動(dòng)脈更適合磁共振成像檢查。動(dòng)物實(shí)驗(yàn)和臨床研究都證實(shí)，HRMRI可以顯示頸動(dòng)脈斑塊的成分和性質(zhì)，對(duì)判斷斑塊的易損性具有非常高的應(yīng)用價(jià)值[11-12]。

2000年，F(xiàn)ayad等最先建立體內(nèi)冠狀動(dòng)脈斑塊的MRI影像檢查方法[5]。冠狀動(dòng)脈與主動(dòng)脈一樣，MRI影像易受到呼吸運(yùn)動(dòng)和心臟跳動(dòng)的影響，且冠狀動(dòng)脈位置較深，走行迂曲，獲取影像更加困難。最初，完成冠狀動(dòng)脈斑塊MRI影像需要屏氣采集，后在提高空間分辨率的同時(shí)成功克服心臟和呼吸的偽影，可在自由呼吸情況下完成[13]。

在外周血管的研究中，2002年Corti等在經(jīng)股動(dòng)脈行經(jīng)皮腔內(nèi)血管成形術(shù)(percutaneous transluminal angioplasty, PTA)后24 h，利用HRMRI橫斷面影像觀察到，動(dòng)脈閉塞層動(dòng)脈粥樣硬化斑塊嚴(yán)重破裂，形成一個(gè)形狀不規(guī)則的內(nèi)腔，進(jìn)一步證實(shí)球囊成形術(shù)可引起斑塊的廣泛破裂，能夠解釋侵入性治療潛在并發(fā)癥的發(fā)生機(jī)制[3]。

2005年，Klein首先證實(shí)HRMRI評(píng)估顱內(nèi)動(dòng)脈粥樣硬化斑塊的有效性，包括大腦中動(dòng)脈和基底動(dòng)脈[6-7]。2010年，Klein等采用增強(qiáng)HRMRI檢查，發(fā)現(xiàn)73%的急性腦橋深部梗死患者的基底動(dòng)脈中存在斑塊，證實(shí)HRMRI可用于分析卒中的病因及發(fā)生機(jī)制，如既往認(rèn)為的腦小血管病變，部分可以重新歸類為繼發(fā)于基底動(dòng)脈粥樣硬化的穿支動(dòng)脈閉塞[14]。

3　HRMRI對(duì)易損斑塊的評(píng)估

與穩(wěn)定斑塊相比，易損斑塊具有較大的脂質(zhì)核心、薄纖維帽、混雜的炎性細(xì)胞以及新生血管形成。臨床上頸動(dòng)脈剝脫術(shù)的樣本可提供有效的組織病理學(xué)依據(jù)。Yuan等研究表明HRMRI能辨別脂質(zhì)核心、斑塊出血和纖維帽，其識(shí)別的斑塊特征與組織學(xué)的結(jié)果有很好的一致性，并進(jìn)一步證實(shí)不穩(wěn)定纖維帽與近期發(fā)生短暫性腦缺血發(fā)作(transient ischemic attack, TIA)或卒中是一致的[1,15-17]。顱內(nèi)動(dòng)脈和頸動(dòng)脈斑塊具有相同的病理特征。應(yīng)用HRMRI評(píng)估腦動(dòng)脈粥樣硬化斑塊的易損性，包括動(dòng)脈重塑、斑塊負(fù)荷、斑塊內(nèi)出血和強(qiáng)化、斑塊分布等特點(diǎn)，具有重要的臨床意義。

3.1動(dòng)脈重塑

動(dòng)脈重塑最早在冠狀動(dòng)脈粥樣硬化的患者中發(fā)現(xiàn)，又稱為Glagov現(xiàn)象[18]。動(dòng)脈重塑有兩種發(fā)展模式，即正性重構(gòu)(positive remodeling, PR)和負(fù)性重構(gòu)(negative remodeling, NR)。正性重構(gòu)表現(xiàn)為血管向外擴(kuò)張，有利于保證血管內(nèi)腔的大小[19]；負(fù)性重構(gòu)則為血管向內(nèi)收縮，會(huì)加重狹窄程度[20-21]。冠狀動(dòng)脈的相關(guān)研究已顯示正性重構(gòu)更多見于癥狀性患者中[22]，這可能是由于正性重構(gòu)在擴(kuò)大管腔面積的同時(shí)增加了斑塊破裂的風(fēng)險(xiǎn)。相反負(fù)性重構(gòu)因富含纖維成分而不易破裂。顱內(nèi)動(dòng)脈研究有相同的發(fā)現(xiàn)，有癥狀的大腦中動(dòng)脈狹窄患者具有較高的正性重構(gòu)，而無癥狀的大腦中動(dòng)脈狹窄患者有更多的負(fù)性重構(gòu)[23]。馬寧等利用HRMRI觀察30例基底動(dòng)脈重度狹窄患者，提示與負(fù)性重構(gòu)相比，正性重構(gòu)占63.3%，且包含較大斑塊[24]。

3.2斑塊負(fù)荷

斑塊的面積被認(rèn)為是顱內(nèi)動(dòng)脈卒中發(fā)生的一個(gè)危險(xiǎn)因素[25-26]。研究表明與無癥狀的大腦中動(dòng)脈狹窄患者相比，有癥狀的大腦中動(dòng)脈狹窄患者具有較大的斑塊厚度。徐蔚海對(duì)照有癥狀和無癥狀大腦中動(dòng)脈狹窄的管壁特點(diǎn)，發(fā)現(xiàn)患者在血管狹窄率相似的情況下，管壁面積具有統(tǒng)計(jì)學(xué)差異，有癥狀的患者管壁面積大，多表現(xiàn)為正性重構(gòu)；而無癥狀的患者管壁面積較小，多表現(xiàn)為負(fù)性重構(gòu)，提示管壁的形態(tài)學(xué)特征可能與癥狀相關(guān)[23]。

3.3斑塊內(nèi)出血

頸動(dòng)脈的研究顯示斑塊內(nèi)出血是缺血性卒中的重要預(yù)測(cè)指標(biāo)[27]。近期一項(xiàng)關(guān)于779例患者隨訪1個(gè)月以上的Meta分析顯示，頸動(dòng)脈MRI顯示斑塊內(nèi)出血作為腦卒中或TIA的預(yù)測(cè)危險(xiǎn)率是4.59(95%CI 2.91～7.24)[28]。Ryu等發(fā)現(xiàn)部分大腦中動(dòng)脈的斑塊在T1WI和/或T2WI圖像中可見局限性高信號(hào)，這種表現(xiàn)更多出現(xiàn)在有癥狀的患者中[26]，依據(jù)頸動(dòng)脈斑塊的研究結(jié)果，推測(cè)可能是一種斑塊內(nèi)出血[29]。徐蔚海等對(duì)109例大腦中動(dòng)脈狹窄(>70%)的患者進(jìn)行回顧性研究，HRMRI發(fā)現(xiàn)斑塊內(nèi)高信號(hào)更多見于有癥狀的患者，而較少見于無癥狀的患者(19.6% vs. 3.2%, P=0.01)[23]。這一結(jié)果與Chen等[30]對(duì)45歲以上大腦中動(dòng)脈粥樣硬化性狹窄病變的尸檢結(jié)果一致。一項(xiàng)關(guān)于74例基底動(dòng)脈狹窄(>50%)患者的研究發(fā)現(xiàn)，有癥狀的損害更多出現(xiàn)在HRMRI發(fā)現(xiàn)斑塊內(nèi)出血陽(yáng)性組中，較少見于陰性組中(80.0% vs. 48.8%, P<0.01)，且斑塊內(nèi)出血多出現(xiàn)在狹窄程度重的患者中[31]。

3.4斑塊的強(qiáng)化

斑塊的強(qiáng)化也與穩(wěn)定性相關(guān)，其表明斑塊內(nèi)血供增加，并且內(nèi)膜的通透性增加促進(jìn)造影劑從血漿進(jìn)入到斑塊內(nèi)。Swartz等首先報(bào)道，對(duì)于顱內(nèi)動(dòng)脈，即使具有多個(gè)狹窄病變，也僅僅在急性腦梗死的責(zé)任血管壁上觀察到斑塊的強(qiáng)化[32]。Skarpathiotakis等證實(shí)在4周內(nèi)發(fā)生缺血性卒中的所有患者，其顱內(nèi)責(zé)任動(dòng)脈斑塊顯示病理性強(qiáng)化，同時(shí)發(fā)現(xiàn)隨著卒中事件發(fā)生時(shí)間的延長(zhǎng)，強(qiáng)化逐漸減弱[33]。Vakil等提供的一項(xiàng)回顧性研究顯示，在有癥狀和無癥狀組之間，斑塊強(qiáng)化具有顯著性差異[34]。該研究中22例重度顱內(nèi)動(dòng)脈狹窄患者，其中70%的癥狀患者斑塊強(qiáng)化，8%的無癥狀患者斑塊強(qiáng)化。婁昕等利用增強(qiáng)HRMRI觀察56例癥狀性基底動(dòng)脈重度狹窄患者的動(dòng)脈管壁情況，結(jié)果認(rèn)為狹窄近端的管壁強(qiáng)化程度與新發(fā)梗死和后期缺血事件相關(guān)[35]。然而，對(duì)于斑塊強(qiáng)化是否可以作為一個(gè)急性缺血性卒中的預(yù)測(cè)因素還存在爭(zhēng)議。少數(shù)患者在急性腦梗死發(fā)生數(shù)月后仍可見強(qiáng)化，是否表明斑塊仍處在不穩(wěn)定狀態(tài)，尚需要進(jìn)一步的前瞻性研究[34]。

3.5斑塊分布

研究表明鑒于顱內(nèi)動(dòng)脈的解剖特點(diǎn)，其斑塊分布研究比顱外動(dòng)脈更具有臨床意義[37]。既往冠狀動(dòng)脈研究發(fā)現(xiàn)，斑塊易形成于血管分支的對(duì)側(cè)壁[38]。徐蔚海利用3.0 T HRMRI觀察中度狹窄的大腦中動(dòng)脈斑塊分布也得出類似結(jié)果，斑塊多位于腹側(cè)壁和下壁，少數(shù)位于背側(cè)壁和上壁[39]。解剖學(xué)研究顯示，大腦中動(dòng)脈的穿支血管多從管壁的背側(cè)壁及上壁發(fā)出[40]。同時(shí)徐蔚海還將有癥狀和無癥狀的患者進(jìn)行對(duì)比，發(fā)現(xiàn)斑塊更多位于血管上壁，較少位于下壁。同時(shí)對(duì)于有癥狀的一組，伴有穿支動(dòng)脈梗死的患者與不伴有穿支動(dòng)脈梗死的患者相比，斑塊也多位于上壁，較少位于腹側(cè)壁和下壁。因此，上壁斑塊更容易導(dǎo)致腦卒中，這可能是由于斑塊更易堵塞穿支血管開口而導(dǎo)致梗死發(fā)生。另外，脫落的栓子也容易進(jìn)入穿支的開口而堵塞下游血管[41]。然而關(guān)于基底動(dòng)脈的一項(xiàng)研究卻與既往大腦中動(dòng)脈斑塊分布規(guī)律不一致。黃飚等利用3.0 T HRMRI觀察38例基底動(dòng)脈狹窄≥30%的有癥狀患者最窄層斑塊的分布，發(fā)現(xiàn)位于腹側(cè)的斑塊最多[42]。臨床解剖發(fā)現(xiàn)基底動(dòng)脈的穿支動(dòng)脈分布于背部和側(cè)壁，腹部沒有穿支分布[43]。這一結(jié)果與解剖結(jié)構(gòu)相矛盾，基底動(dòng)脈的斑塊分布特點(diǎn)還需要進(jìn)一步的相關(guān)研究。

4　存在問題及展望

目前，在動(dòng)脈粥樣硬化斑塊的觀察研究中，HRMRI得到廣泛應(yīng)用。同時(shí)，通過HRMRI可以明確斑塊位置與穿支動(dòng)脈關(guān)系，指導(dǎo)臨床上對(duì)于缺血性卒中的病因分型和介入治療，避免支架植入后引起穿支動(dòng)脈閉塞[44]。然而，HRMRI仍存在不足，首先，一些患者因?yàn)橛拈]恐懼癥、體內(nèi)有心臟起搏器或除顫器、動(dòng)脈瘤夾等金屬物而無法進(jìn)入磁共振成像環(huán)境。其次，為了分辨斑塊成分，獲取高空間分辨率需要較高的信噪比和較長(zhǎng)的掃描成像時(shí)間。此外，HRMRI評(píng)估斑塊形態(tài)通常局限于單個(gè)斑塊或血管段，不能評(píng)估大段的動(dòng)脈系統(tǒng)。

未來，希望能夠在臨床醫(yī)師和影像專家的共同努力下，建立一個(gè)可以定量評(píng)估斑塊成分的方法和自動(dòng)化分析軟件。同時(shí)通過對(duì)斑塊的定量和定性的檢測(cè)能夠鑒定高危斑塊，明確患者的高危分層，精準(zhǔn)預(yù)測(cè)腦血管事件的發(fā)生。

[參考文獻(xiàn)]

[1] Yuan C, Mitsumori LM, Ferguson MS, et al. In vivo accuracy of multispectral magnetic resonance imaging for identifying lipid- rich necrotic cores and intraplaque hemorrhage in advanced human carotid plaques [J]. Circulation, 2001, 104(17): 2051-2056.

[2] Fayad ZA, Nahar T, Fallon JT, et al. In vivo magnetic resonance evaluation of atherosclerotic plaques in the human thoracic aorta: a comparison with transesophageal echocardiography [J]. Circulation, 2000, 101(21): 2503-2509.

[3] Corti R, Wyttenbach R, Alerci M, et al. Images in cardiovascular medicine. Effect of percutaneous transluminal angioplasty on severely stenotic femoral lesions: in vivo demonstration by noninvasive magnetic resonance imaging [J]. Circulation, 2002, 106(12): 1570-1571.

[4] Coulden RA, Moss H, Graves MJ, et al. High resolution magnetic resonance imaging of atherosclerosis and the response to balloon angioplasty [J]. Heart, 2000, 83(2): 188-191.

[5] Fayad ZA, Fuster V, Fallon JT, et al. Noninvasive in vivo human coronary artery lumen and wall imaging using black- blood magnetic resonance imaging [J]. Circulation, 2000, 102(5): 506-510.

[6] Klein IF, Lavallee PC, Touboul PJ, et al. In vivo middle cerebral artery plaque imaging by high-resolution MRI [J]. Neurology, 2006, 67(2): 327-329.

[7] Klein IF, Lavallee PC, Schouman-Claeys E, et al. High-resolution MRI identifies basilar artery plaques in paramedian pontine infarct [J]. Neurology, 2005, 64(3): 551-552.

[8] Ryu CW, Kwak HS, Jahng GH, et al. High-resolution MRI of intracranial atherosclerotic disease [J]. Neurointervention, 2014, 9(1): 9-20.

[9] Fayad ZA, Fuster V. Characterization of atherosclerotic plaques by magnetic resonance imaging [J]. Ann N Y Acad Sci, 2000, 902: 173-186.

[10] Toussaint JF, LaMuraglia GM, Southern JF, et al. Magnetic resonance images lipid, fibrous, calcified, hemorrhagic, and thrombotic components of human atherosclerosis in vivo [J]. Circulation, 1996, 94(5): 932-938.

[11] Saam T, Hatsukami TS, Takaya N, et al. The vulnerable, or high-risk, atherosclerotic plaque: noninvasive MR imaging for characterization and assessment [J]. Radiology, 2007, 244(1): 64-77.

[12] Li M, Le WJ, Tao XF, et al. Advantage in bright-blood and black-blood magnetic resonance imaging with high-resolution for analysis of carotid atherosclerotic plaques [J]. Chin Med J (Engl), 2015, 128(18): 2478-2484.

[13] Botnar RM, Stuber M, Kissinger KV, et al. Noninvasive coronary vessel wall and plaque imaging with magnetic resonance imaging [J]. Circulation, 2000, 102(21): 2582-2587.

[14] Klein IF, Lavallée PC, Mazighi M, et al. Basilar artery atherosclerotic plaques in paramedian and lacunar pontine infarctions: a high- resolution MRI study [J]. Stroke, 2010, 41(7): 1405-1409.

[15] Cai J, Hatsukami TS, Ferguson MS, et al. In vivo quantitativemeasurement of intact fibrous cap and lipid-rich necrotic core size in atherosclerotic carotid plaque: comparison of high-resolution, contrast-enhanced magnetic resonance imaging and histology [J]. Circulation, 2005, 112(22): 3437-3444.

[16] Mitsumori LM, Hatsukami TS, Ferguson MS, et al. In vivo accuracy of multisequence MR imaging for identifying unstable fibrous caps in advanced human carotid plaques [J]. J Magn Reson Imaging, 2003, 17(4): 410-420.

[17] Yuan C, Zhang SX, Polissar NL, et al. Identification of fibrous cap rupture with magnetic resonance imaging is highly associated with recent transient ischemic attack or stroke [J]. Circulation, 2002, 105(2): 181-185.

[18] Glagov S, Weisenberg E, Zarins CK, et al. Compensatory enlargement of human atherosclerotic coronary arteries [J]. N Engl J Med, 1987, 316(22): 1371-1375.

[19] Kim YS, Lim SH, Oh KW, et al. The advantage of high-resolution MRI in evaluating basilar plaques: acomparison study with MRA[J].Atherosclerosis, 2012, 224(2): 411-416.

[20] Nishioka T, Luo H, Eigler NL, et al. Contribution of inadequate compensatory enlargement to development of human coronary artery stenosis: an in vivo intravascular ultrasound study [J]. JAm Coll Cardiol, 1996, 27(7): 1571-1576.

[21] Pasterkamp G, Wensing PJ, Post MJ, et al. Paradoxical arterial wall shrinkage may contribute to luminal narrowing of human atherosclerotic femoral arteries [J]. Circulation, 1995, 91 (5): 1444-1449.

[22] Schoenhagen P, Ziada KM, Kapadia SR, et al. Extent and direction of arterial remodeling in stable versus unstable coronary syndromes: an intravascular ultrasound study [J]. Circulation, 2000, 101(6): 598-603.

[23] Xu WH, Li ML, Gao S, et al. In vivo high-resolution MR imaging of symptomatic and asymptomatic middle cerebral artery atherosclerotic stenosis [J]. Atherosclerosis, 2010, 212(2): 507-511.

[24] Ma N, Jiang WJ, Lou X, et al. Arterial remodeling of advanced basilar atherosclerosis: a 3-tesla MRI study [J]. Neurology, 2010, 75(3): 253-258.

[25] Chung GH, Kwak HS, Hwang SB, et al. High resolution MR imaging in patients with symptomatic middle cerebral artery stenosis [J]. Eur J Radiol, 2012, 81(12): 4069-4074.

[26] Ryu CW, Jahng GH, Kim EJ, et al. High resolution wall and lumen MRI of the middle cerebral arteries at 3 tesla [J]. Cerebrovasc Dis, 2009, 27(5): 433-442.

[27] Saam T, Hetterich H, Hoffmann V, et al. Meta-analysis and systematic review of the predictive value of carotid plaque hemorrhage on cerebrovascular events by magnetic resonance imaging [J]. JAm Coll Cardiol, 2013, 62(12): 1081-1091.

[28] Gupta A, Baradaran H, Schweitzer AD, et al. Carotid plaque MRI and stroke risk: a systematic review and meta- analysis [J]. Stroke, 2013, 44(11): 3071-3077.

[29] Kampschulte A, Ferguson MS, Kerwin WS, et al. Differentiation of intraplaque versus juxtaluminal hemorrhage/thrombus in advanced human carotid atherosclerotic lesions by in vivo magnetic resonance imaging [J]. Circulation, 2004, 110(20): 3239-3244.

[30] Chen XY, Wong KS, Lam WWM, et al. Middle cerebral artery atherosclerosis: histological comparison between plaques associated with and not associated with infarct in a postmortem study [J]. Cerebrovasc Dis, 2008, 25(1-2): 74-80.

[31] Yu JH, Kwak HS, Chung GH, et al. Association of intraplaque hemorrhage and acute infarction in patients with basilar artery plaque [J]. Stroke, 2015, 46(10): 2768-2772.

[32] Swartz RH, Bhuta SS, Farb RI, et al. Intracranial arterial wall imaging using high- resolution 3- tesla contrast- enhanced MRI [J]. Neurology, 2009, 72(7): 627-634.

[33] Skarpathiotakis M, Mandell DM, Swartz RH, et al. Intracranial atherosclerotic plaque enhancement in patients with ischemic stroke [J].AJNRAm J Neuroradiol, 2013, 34(2): 299-304.

[34] Vakil P, Vranic J, Hurley MC, et al. T1 gadolinium enhancement of intracranial atherosclerotic plaques associated with symptomatic ischemic presentations [J]. AJNR Am J Neuroradiol, 2013, 34(12): 2252-2258.

[35] Lou X, Ma N, Ma L, et al. Contrast-enhanced 3T high-resolution MR imaging in symptomatic atherosclerotic basilar artery stenosis [J].AJNRAm Neuroradiol, 2013, 34(3): 513-517.

[36] Vergouwen MDI, Silver FL, Mandell DM, et al. Fibrous cap enhancement in symptomatic atherosclerotic basilar artery stenosis [J].Arch Neurol, 2011, 68(5): 676.

[37] Watanabe H, Yoshida K, Akasaka T, et al. Intravascular ultrasound assessment of plaque distribution in the ostium of the left anterior descending coronary artery [J]. Am J Cardiol, 1996, 78(7): 827-829.

[38] Marinkovic SV, Milisavljevic MM, Kovacevic MS, et al. Perforating branches of the middle cerebral artery. Microanatomy and clinical significance of their intracerebral segments [J]. Stroke, 16(6): 1022-1029.

[39] Xu WH, Li ML, Gao S, et al. Plaque distribution of stenotic middle cerebral artery and its clinical relevance [J]. Stroke, 2011, 42(10): 2957-2959.

[40] Umansky F, Gomes FB, Dujovny M, et al. The perforating branches of the middle cerebral artery. A microanatomical study [J]. J Neurosurg, 1985, 62(2): 261-268.

[41] Ryoo S, Lee MJ, Cha J, et al. Differential vascular pathophysiologic types of intracranial atherosclerotic stroke: a high-resolution wall magnetic resonance imaging study [J]. Stroke, 2015, 46(10): 2815-2821.

[42] Huang B, Yang WQ, Liu XT, et al. Basilar artery atherosclerotic plaques distribution in symptomatic patients: a 3.0 T high- resolution MRI study [J]. Eur J Radiol, 2013, 82(4): 199-203.

[43] Saeki N, Rhoton AL Jr. Microsurgical anatomy of the upper basilar artery and the posterior circle of Willis [J]. J Neurosurg, 1977, 46(5): 563-578.

[44] Jiang WJ, Yu W, Ma N, et al. High resolution MRI guided endovascular intervention of basilar artery disease [J]. J Neurointerv Surg, 2011, 3(4): 375-378.

Progress of High-resolution Magnetic Resonance Imaging in Evaluating Cerebral Atherosclerotic Plaques (review)

YU Jin1,2a, BAI Xiao2b, WU Shi-wen2a, XU Wei-hai3, WU Wei-ping1
1. Department of Geriatric Neurology, People's Liberation Army General Hospital, Beijing 100853, China; 2. a. Department of Neurology; b. Department of Cadre Ward, General Hospital of Chinese People's Armed Police Forces, Beijing 100039, China; 3. Department of Neurology, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences, Beijing 100730, China

Correspondence to WU Wei-ping. E-mail: wuwp@vip.sina.com

Abstract:High-resolution magnetic resonance imaging (HRMRI) is a safe, non-invasive, inexpensive, accurate and reproducible clinical imaging modality, and the results can acutely reflect the extent of atherosclerotic disease and have high predictive values for future clinical events. It uses black blood imaging techniques and can obtain sufficient sensitivity for submillimetre imaging. HRMRI has been used widely to visualize the vessel wall and differentiate the components of atherosclerotic plaques. It is of important clinical meaning to evaluate plaque vulnerability with HRMRI, which is related to the remodeling pattern, plaque burden, intraplaque hemorrhage and contrast enhancement, and plaque distribution, etc.

Key words:high-resolution; magnetic resonance imaging; cerebral arteries; atherosclerosis; plaque; review

(收稿日期：2015-11-02修回日期：2015-12-01)

DOI:10.3969/j.issn.1006-9771.2016.02.009

[中圖分類號(hào)]R543.5

[文獻(xiàn)標(biāo)識(shí)碼]A

[文章編號(hào)]1006-9771(2016)02-0164-04