Abstract
目的
分别采用高分辨率磁共振成像(high-resolution magnetic resonance imaging,HR-MRI)和颅脑三维伪连续动脉自旋标记(3D pseudo-continuous arterial spin labeling,3D pcASL)分析单侧颈动脉中重度狭窄患者斑块特征与脑血流量(cerebral blood flow,CBF)的相关性。
方法
选择43例单侧颈动脉中重度狭窄患者,采用HR-MRI分别测量颈动脉狭窄程度、最大管壁厚度(maximum wall thickness,Max WT)、标准化管壁指数(normalized wall index,NWI),进行斑块特征分析,记录有无斑块内出血(intraplaque hemorrhage,IPH)、富脂坏死核(lipid-rich necrotic nuc-leus,LRNC)、钙化和溃疡,以及钙化和LRNC分级。采用3D pcASL测量双侧大脑中动脉供血区内感兴趣区的CBF值。采用配对样本t检验比较患侧和对侧CBF值差异,采用Spearman相关分析比较患侧颈动脉狭窄程度、Max WT、NWI与CBF值的相关性,采用Mann-Whitney U检验比较斑块成分中有无IPH、溃疡时CBF值的差异,采用Kruskal-Wallis检验比较不同级别钙化、LRNC时CBF值差异。
结果
患侧颈动脉平均狭窄程度为77.30%±11.79%。患侧和对侧平均CBF值分别为(46.77±11.65) mL/(100 g·min)和(49.92±9.95) mL/(100 g·min),差异有统计学意义(t=-2.474,P=0.017)。患侧颈动脉斑块平均Max WT为(6.40±1.87) mm,平均NWI为62.91%±8.87%。患侧颈动脉狭窄程度、Max WT、NWI与CBF值未见明显相关(P>0.05)。斑块成分分析显示,患侧斑块内有无钙化及钙化程度不同时,CBF值有差异(P=0.030),有无IPH、溃疡及LRNC时的患侧CBF值差异无统计学意义。
结论
单侧颈动脉中重度狭窄患者中,斑块内钙化可能影响脑血流灌注,当无钙化存在时,需要特别关注斑块成分。
Keywords: 动脉粥样硬化斑块, 颈动脉狭窄, 血管钙化, 磁共振成像, 脑血流
Abstract
Objective
To investigate the correlations between carotid plaque characteristics and cerebral blood flow (CBF) in patients with unilateral moderate to severe carotid stenosis using high-resolution magnetic resonance imaging (HR-MRI) and 3D pseudo-continuous arterial spin labeling (3D pcASL).
Methods
A total of 43 patients with unilateral moderate to severe carotid stenosis were recruited. The degree of carotid stenosis, maximum wall thickness (Max WT) and normalized wall index (NWI) were measured using HR-MRI. The plaque characteristics were analyzed. Presence or absence of plaque components including intraplaque hemorrhage (IPH), lipid-rich necrotic nucleus (LRNC), calcification and ulcer were identified, and the grades of calcification and LRNC were recorded. CBF values within the region of interest representing the bilateral middle cerebral artery distribution were acquired using 3D pcASL. Paired sample t test was used to compare the differences of CBF values between the index side and the contralateral side. Spearman correlation analysis was conducted to evaluate the correlations of CBF values with the degree of carotid stenosis, Max WT and NWI. The differences of CBF values between the patients with or without IPH and ulcer were compared using Mann-Whitney U test. Different levels of calcification and LRNC were compared by Kruskal-Wallis test, respectively.
Results
The ave-rage degree of carotid stenosis at the index side was 77.30%±11.79%. The mean CBF value of the index side was (46.77±11.65) mL/(100 g·min), and that of the contralateral side was (49.92±9.95) mL/(100 g·min), and the difference was statistically significant (t=-2.474, P=0.017). The mean Max WT and NWI of the carotid plaques at the index side was (6.40±1.87) mm and 62.91%±8.87%, respectively. There were no significant correlations of CBF values with the degrees of stenosis, Max WT and NMI (P>0.05). Plaque composition analysis showed that the CBF values of the index side were different when there was calcification or not and the degrees of calcification were different (P=0.030), but there were no differences between the CBF values on the index sides with or without IPH, ulcer and LRNC.
Conclusion
In patients with unilateral moderate to severe carotid stenosis, calcification might affect CBF perfusion. When there is no calcification, the plaque components need attention.
Keywords: Atherosclerotic plaque, Carotid stenosis, Vascular calcification, Magnetic resonance imaging, Cerebral blood flow
颈动脉粥样硬化性狭窄与脑卒中密切相关。目前,多种方法可以测量颈动脉管腔狭窄程度,但仅评估管腔狭窄程度可能会低估动脉粥样硬化的严重性。动脉粥样硬化斑块根据成分特征可以分为稳定斑块和易损斑块,其中易损斑块存在斑块破裂的风险[1],因此,对斑块成分进行详细分析极为重要。
高分辨率磁共振成像(high-resolution magnetic resonance imaging,HR-MRI)是能直观反映颈动脉管壁结构及斑块内部形态、大小、成分等的无创性方法[2-7]。目前已有不少研究使用HR-MRI进行斑块成分分析[8-11],研究多关注易损斑块,包括较大富脂坏死核(lipid-rich necrotic nucleus,LRNC)、薄纤维帽、活化的炎性细胞聚集、斑块破裂、斑块内出血(intraplaque hemorrhage,IPH)等[12]。三维伪连续动脉自旋标记(3D pseudo-continuous arterial spin labeling,3D pcASL)是无创性获得脑血流灌注及定量测量脑血流量(cerebral blood flow,CBF)的成像方法,适合用于术前检查和术后随访;其采用水作为内源性对比剂标记动脉,可获得全脑脑血流灌注[13],且具有较高的信噪比和图像质量。本研究即将上述两种方法结合,选择LRNC、IPH、钙化和溃疡作为评估点,评估斑块特征和脑血流灌注的相关性。
1. 资料与方法
1.1. 研究对象
选择2019年5月至2020年1月于北京大学第三医院神经外科行颈动脉内膜切除术的患者,所有患者均行颈动脉超声诊断为单侧颈动脉中重度狭窄(狭窄程度50%~99%),对侧颈动脉未见狭窄或轻度狭窄(狭窄程度小于50%),且均行头颈动脉计算机断层血管造影(computed tomography angiography, CTA)确定颈动脉及颅内血管情况。排除颈内动脉颅内段或颅内动脉重度狭窄/闭塞、近期新发出血性脑梗死、颅内出血、脑肿瘤及有磁共振检查禁忌证患者。最终有43例纳入本研究,包括男性40例,女性3例,年龄60~85岁,平均(69.1±6.2)岁。其中39例为有症状性颈动脉狭窄(表现为黑朦、卒中或其他相关神经症状等),4例为体检发现颈动脉狭窄;26例有高血压病史,28例有高脂血症病史,14例有糖尿病病史,4例有冠心病病史,26例有吸烟史,26例有饮酒史。所有患者均知情同意。
1.2. HR-MRI和3D pcASL检查方法
所有患者均在3.0 T磁共振(联影,uMR780)下,使用8通道颈动脉线圈行颈动脉HR-MRI扫描,以中重度狭窄侧为患侧,另一侧为对侧。扫描序列:(1)3D时间飞跃法(time of flight,TOF):重复时间(repetition time,TR)/回波时间(echo time,TE)=17.6 ms/6.7 ms,翻转角8°,层厚2 mm;(2)2D T1WI:TR/TE=850 ms/13.44 ms,层厚2 mm;(3)2D T2WI:TR/TE=2 000 ms/96.6 ms,层厚2 mm;(4)同步非对比剂血管成像和斑块内出血成像(simultaneous non-contrast angiography intraplaque hemorrhage,SNAP):TR/TE=9.6 ms/4.0 ms,翻转角12°,层厚1 mm。所有序列视场(field of view,FOV)=140 mm×140 mm,分辨率0.55 mm× 0.55 mm,扫描范围32 mm。
所有患者均在HR-MRI检查后1周内,在3.0 T磁共振(GE,750)下,使用8通道头线圈完成颅脑3D pcASL序列扫描。扫描参数:TR/TE=4 632 ms/10.5 ms,层厚4 mm,层间距0 mm,体素大小2 mm×2 mm×4 mm,标记后延迟时间(post-labeling delay,PLD)为2.0 s,覆盖全脑,总时长为3分45秒。
1.3. 图像处理及数据分析
由两名从事神经放射学专业两年以上放射科医师完成图像处理及数据分析,当结果不一致时,由第三名从事神经放射学专业10年以上的放射科医师复核,研究者对患者的临床信息及颅内外血管状态等信息均不知情。在3D TOF图像上按照北美症状性颈动脉内膜切除术试验(North American sympto-matic carotid endarterectomy trial,NASCET)评价颈动脉的狭窄程度,即狭窄程度=(1-最狭窄处直径/远端正常直径)×100%,计算并记录患侧管腔狭窄程度。使用软件Vessel Explorer 2(TSimaging Healthcare,China)勾画患侧颈动脉管腔和管壁,并计算最大管壁厚度(maximum wall thickness,Max WT)和标准化管壁指数(normalized wall index,NWI)。
分析颈动脉斑块成分,根据情况进行分级评分:IPH和溃疡,根据有无分别记录为1分(有)、0分(无);钙化,根据有无及最大厚度分别记录为2分(厚度≥2 mm)、1分(厚度 < 2 mm)、0分(无);LRNC,根据有无及最大截面积占比分别记录为2分(最大截面积占比≥50%)、1分(最大截面积占比 < 50%)、0分(无)。
3D pcASL原始图像传至设备后处理工作站(GE ADW 4.7),利用后处理软件获得脑血流灌注图像。选择双侧大脑中动脉供血区为感兴趣区(region of interest,ROI),分别测量患侧和对侧的CBF值,各测量3次取平均值记录。
1.4. 统计学分析
采用SPSS 19.0软件(Inc.,IL,USA)完成统计分析。如数据符合正态分布,采用t检验或方差分析,否则采用非参数检验。采用配对样本t检验比较患侧和对侧CBF值;采用Mann-Whitney U检验比较有无IPH、溃疡时患侧和对侧CBF值;采用Kruskal-Wallis检验分析不同分级LRNC、钙化的患侧和对侧CBF值。采用Spearman相关分析比较患侧颈动脉狭窄程度、Max WT和NWI与CBF值的相关性。P < 0.05为差异有统计学意义。
2. 结果
2.1. 颈动脉狭窄程度
43例患者的患侧颈动脉狭窄程度在51.02%~99.00%,平均狭窄程度为77.30%±11.79%。
2.2. 颈动脉斑块情况
本组患者颈动脉斑块情况见表 1,患侧颈动脉斑块Max WT为(6.40±1.87) mm,平均NWI为62.91%±8.87%。
表 1.
不同颈动脉斑块成分占比
Proportion of carotid plaque components
Plaque characteristics | Score 0 | Score 1 | Score 2 |
Data are expressed as n(%). | |||
Intraplaque hemorrhage | 21 (48.84) | 22 (51.16) | |
Lipid-rich necrotic nucleus | 5 (11.63) | 11 (25.58) | 27 (62.79) |
Calcification | 8 (18.60) | 25 (58.14) | 10 (23.26) |
Ulcer | 12 (27.91) | 31 (72.09) |
2.3. 脑血流灌注情况
43例患者患侧大脑中动脉供血区CBF值低于对侧,差异有统计学意义[(46.77±11.65) mL/(100 g·min) vs. (49.92±9.95) mL/(100 g·min),t=-2.474,P=0.017]。相关性分析提示,患侧颈动脉狭窄程度、Max WT、NWI与CBF值之间未见明显相关(表 2)。
表 2.
患侧颈动脉形态特征与脑血流量的相关性
Correlation between carotid artery morphology and cerebral blood flow of the index side
Variable | Correlation coefficient | P value |
Max WT, maximum wall thickness; NWI, normalized wall index. | ||
Degree of carotid stenosis | -0.106 | 0.499 |
Max WT | 0.158 | 0.311 |
NWI | -0.017 | 0.913 |
患侧CBF值在不同钙化评分间差异有统计学意义(P=0.030,表 3),而对侧CBF值在不同钙化评分间差异无统计学意义(P=0.443)。进一步组间两两比较发现,钙化评分0分的患侧CBF值低于1分和2分(图 1和2),但仅0分和1分之间的患侧CBF值差异有统计学意义(P=0.024),0分和2分、1分和2分之间差异均无统计学意义(P=0.337,P=0.306)。患侧和对侧CBF值在有无IPH间及有无溃疡间差异均无统计学意义,在不同LRNC评分间差异亦无统计学意义(P>0.05,表 3)。
表 3.
不同颈动脉斑块成分评分的患侧脑血流量
Cerebral blood flow on the index side in different carotid plaque component scores
Plaque characteristics | Score 0 | Score 1 | Score 2 | P value |
Data are expressed as x±s. | ||||
Intraplaque hemorrhage | 47.04±10.80 | 46.52±12.66 | 0.662 | |
Lipid-rich necrotic nucleus | 53.57±14.61 | 45.79±10.01 | 45.92±11.75 | 0.528 |
Calcification | 39.27±11.89 | 46.64±10.42 | 53.11±11.81 | 0.030 |
Ulcer | 46.10±12.67 | 48.52±8.72 | 0.565 |
图 1.
右侧颈内动脉起始处钙化斑块与脑血流灌注
Calcified plaque at the beginning of right internal carotid artery and ipsilateral cerebral blood flow perfusion
A, 3D T1WI CPR showed calcified plaque was at the beginning of right internal carotid artery with severe stenosis; B, TOF, SNAP, T1WI and T2WI sequences showed calcified plaque (white arrow) on the wall of internal carotid artery, and low signals were found on all sequences; C, cerebral blood flow(CBF) map showed that there was no significant change of CBF perfusion on the middle cerebral artery distribution of the index side. CPR, curved plannar reformation; MR, magnetic resonance; ASL, arterial spin labeling; TOF, time of flight; SNAP, simultaneous non-contrast angiography intraplaque hemorrhage.
图 2.
右侧颈内动脉起始处无钙化成分的斑块与脑血流灌注
Plaque without calcification at the beginning of right internal carotid artery and ipsilateral cerebral blood flow perfusion
A, 3D T1WI CPR showed plaque without calcified at the beginning of right internal carotid artery with severe stenosis; B, TOF, SNAP, T1WI and T2WI sequences showed plaque without calcified (white asterisk showed lumen); C, CBF map showed that CBF perfusion of the right middle cerebral artery distribution was significantly decreased. Abbreviations as in Figure 1.
3. 讨论
3.1. 颈动脉斑块形态特征与脑血流灌注
颈动脉管腔狭窄程度测量是目前常用来评估颈动脉粥样硬化病变严重性的方法之一。但是由于血管壁的正性重构作用,即使斑块体积已经明显增大,管腔面积仍可很长时间保持不变,单纯测量狭窄程度可能无法准确评估动脉粥样硬化病变程度。Max WT和NWI是斑块负荷特征的两项重要指标,本研究通过评估颈动脉狭窄程度、斑块负荷特征与脑血流灌注的相关性,判断是否可通过颈动脉斑块形态特征的分析来预测脑血流灌注的改变。相关分析显示,颈动脉狭窄程度不同的患侧和对侧,CBF值已经出现了变化,患侧CBF值较对侧下降,而患侧颈动脉狭窄程度、Max WT和NWI与同侧脑血流灌注未见明显相关。原因考虑为本组患者均为慢性颈动脉狭窄患者,管腔逐步狭窄,致患侧CBF值下降,但由于侧支循环形成或对侧代偿,脑血流灌注下降程度与斑块形态未呈现显著相关。在临床中,很多患者往往不是急性颈动脉狭窄,慢性狭窄更为常见,因此,不能仅通过斑块形态特征来判断评估脑血流灌注变化。
3.2. 颈动脉斑块成分特征与脑血流灌注
关于颈动脉斑块内钙化对脑血流灌注的影响,目前研究尚不明确。既往认为钙化斑块比非钙化斑块稳定,但也有研究报道重度颈动脉狭窄患者中,具有较高钙化负荷的斑块内出血性成分更多,而脂质核心较少,提示钙化可能为不稳定因素[14]。斑块表面钙化更易导致斑块破损,增加斑块破裂风险。高密度钙化在CT血管造影上分析时会出现过度评估情况,对管腔直径测量产生一定影响,从而影响对管腔狭窄程度的判断。斑块内钙化在HR-MRI管壁成像的多个序列均为低信号,管腔内部结构可以清晰显示,对颈动脉管腔直径测量影响较小。本研究根据钙化有无及其厚度将患者分为三级,发现不同级间患侧脑血流灌注存在明显差异,即有钙化斑块者其脑血流灌注较没有钙化斑块者高,考虑原因可能为动脉粥样硬化斑块的形成是一种慢性脂质驱动血管壁炎性疾病,从血管内膜下脂质沉积开始,伴随着巨噬细胞吞噬脂质从而形成泡沫细胞,钙盐的沉积主要发生在斑块形成晚期,钙化的形成意味着斑块的长期进展。斑块长期进展过程中,各种代偿机制,包括Willis环等侧支循环逐步形成并完善,这或许可以解释脑血流灌注的部分代偿。由于本研究分组后病例数量较少,尽管存在统计学差异,但仅能初步提示存在钙化的斑块可能更稳定,与不存在钙化的斑块相比,CBF值下降的程度更小,因此,对于不存在钙化的斑块,当CBF值出现下降趋势时更需密切关注。
LRNC在绝大部分颈动脉斑块成分研究中均被选定为研究对象,研究显示其可能引起脑血流灌注改变[15-17]。Underhill等[15]发现LRNC可能为较早出现的斑块危险因素,可以单独作为预测出血及纤维帽破裂的指标。Qiao等[16]发现,当LRNC增大时,管壁厚度明显增加,增大了斑块负担和不稳定性,可能导致斑块破裂风险增加,脑血流灌注下降,从而增加卒中风险。本研究根据LRNC有无及最大截面积占比进行分级,发现无论有无LRNC以及LRNC不同分级间,患侧脑血流灌注差异均无统计学意义,说明当LRNC含量增多时,并未引起管腔血流灌注的减低。究其原因可能有如下两个方面:一方面,本研究纳入病例均为颈动脉中重度狭窄患者,斑块负荷增加过程中伴随着代偿机制发生,即使LRNC的出现增加了斑块不稳定性,但尚未对脑血流灌注产生具有统计学差异的影响。曾有研究表明侧支循环在维持颅外动脉狭窄患者脑血流灌注中发挥着重要作用[18],Jones等[19]的研究也显示单侧颈动脉狭窄患者患侧大脑中动脉接受对侧血流供应。另一方面,斑块内各成分体积是影响脑血流灌注的指标,本研究未对其进行定量分析,这可能也是影响该结果的原因之一。
SNAP序列对于斑块内出血的显示有较高特异性和敏感性[20]。多项研究显示IPH与脑血流灌注下降存在相关性,因此有学者认为,相较于脂质核,IPH是与斑块易损性更相关的指标[21-22],微栓子脱落可进一步导致微循环破坏。另有研究表明,随着IPH体积的增加,急性脑梗死的发生率明显增加[23]。本研究得出有无IPH的患侧脑血流灌注并无明显差别,考虑与文献并不一致的原因可能为,尽管在IPH的刺激下,局部斑块体积明显增大,管腔截面积下降,通过血流减少,但相应脑血流灌注存在较强代偿作用,当处于代偿阶段时,IPH体积的进一步增大并未引起CBF值明显下降。
本研究尚有不足之处:首先,样本数较少,得到的统计学结果有待扩大样本量进一步验证;其次,手动勾画ROI的方法存在一定的手工选择性差异;再次,仅对不同斑块内成分进行分级评分,未进一步对斑块内成分的体积进行定量分析;最后,颅内侧支循环状态是影响颈动脉狭窄患者脑血流灌注的因素,血管选择性动脉自旋标记技术(territorial arterial spin labeling,tASL)可以对单支血管进行标记,得到不同供血动脉脑血流灌注及侧支循环情况,将来可考虑结合tASL进行进一步分析。
总之,单侧颈动脉中重度狭窄患者斑块内钙化可能影响脑血流灌注,当无钙化存在时,需要特别关注斑块成分。在设备允许情况下,无创的颈动脉HR-MRI结合3D pcASL技术可以一次性完成颈动脉和脑血流灌注的评估分析,对颈动脉粥样硬化性狭窄患者的诊疗提供了有力的影像学支持。
Funding Statement
北京市自然科学基金(7192219)
Supported by Beijing Natural Science Foundation (7192219)
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