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临床研究
伪连续动脉自旋标记成像评估出血型烟雾病患者脑血流动力学研究
王宪雯 吴芳 刘玥宏 王二玲 范文涛 张献昌 姚泽山 杨旗

Cite this article as: Wang XW, Wu F, Liu YH, et al. Study of pseudo-continuous arterial spin labeling perfusion MRI on the evaluation of cerebral hemodynamics in patients with hemorrhagic moyamoya disease[J]. Chin J Magn Reson Imaging, 2022, 13(1): 6-10.本文引用格式:王宪雯, 吴芳, 刘玥宏, 等. 伪连续动脉自旋标记成像评估出血型烟雾病患者脑血流动力学研究[J]. 磁共振成像, 2022, 13(1): 6-10. DOI:10.12015/issn.1674-8034.2022.01.002.


[摘要] 目的 基于伪连续动脉自旋标记成像(pseudo-continuous arterial spin labeling,pCASL)技术探讨成人烟雾病出血后脑血流动力学改变。材料与方法 将首都医科大学附属宣武医院2016年12月至2019年4月收治的32例出血型或缺血型成人烟雾病患者共计38个阳性征象半球作为研究对象,其中出血半球21个、缺血半球17个,均在发病3个月内进行pCASL检查,在半卵圆中心层面及阳性征象层面选取病变周围区域、同侧额叶、颞叶进行感兴趣区测算获得pCASL-脑血流量(cerebral blood flow,CBF)、pCASL-动脉脑血容量(arterial cerebral blood volume,aCBV)、pCASL-动脉通过时间(arterial transit time,ATT)数值,出血组和缺血组组间比较,采用两独立样本t检验和Mann-Whitney U检验。结果 (1)出血型大脑半球共计21个,病变周围测算aCBV、ATT及CBF分别为(1.01±0.22) mL/100g、(1.53±0.98) s和(37.88±6.19) mL/(100 g·min),额叶测算aCBV、ATT及CBF分别为(1.23±0.31) mL/100g、(1.55±0.15) s和(47.03±13.78) mL/(100 g·min),颞叶测算aCBV、ATT及CBF分别为(1.28±0.30) mL/100g、(1.54±0.12) s和(51.91±13.96) mL/(100 g·min);缺血型大脑半球共计17个,病变周围测算aCBV、ATT及CBF分别为(1.11±0.24) mL/100g、(1.46±0.35) s和(49.27±14.13) mL/(100 g·min),额叶测算aCBV、ATT及CBF分别为(1.17±0.30) mL/100g、(1.51±0.37) s和(43.17±14.63) mL/(100 g·min),颞叶测算aCBV、ATT及CBF分别为(1.21±0.35) mL/100g、(1.50±0.40) s和(49.25±20.85) mL/(100 g·min)。(2)出血型与缺血型相比,病变周围区CBF值显著减低,差异有统计学意义(P<0.05),aCBV及ATT差异无统计学意义,额叶及颞叶pCASL灌注差异无统计学意义。结论 出血型烟雾病患者pCASL上脑灌注较缺血型烟雾病更低,pCASL可以检测成人出血型烟雾病患者的血流衰竭程度,监测周围额颞叶细微的缺血变化,为进一步通过监测血流动力学情况预警再出血发生提供研究基础。
[Abstract] Objective To investigate hemodynamic changes in adult patients with hemorrhagic moyamoya disease based on pseudo-continuous artery spin labeling (pCASL) imaging.Materials and Methods: A total of 32 patients (38 hemispheres) with hemorrhagic or ischemic moyamoya diasease in Xuanwu Hospital were enrolled from December 2016 to April 2019, including 21 hemorrhagic hemispheres and 17 ischemic hemispheres. All patients underwent pCASL exams within 3 months after the onset. Mean perfusion parameters of cerebral blood flow (CBF), pCASL-arterial cerebral blood volume (aCBV) and pCASL-arterial transit time (ATT) derived using pCASL were measured within peripheral region of the lesion, ipsilateral frontal lobe and temporal lobe on the semi-oval layer and positive lesion layer. Inter-group comparison between hemorrhage and infarction was carried out through t-test of two independent samples and Mann-Whitney U test of two independent samples.Results A total of 21 hemorrhagic hemispheres were involved. In the peripheral region of the lesion, mean aCBV, ATT and CBF values were (1.01±0.22) mL/100g, (1.53±0.98) s and (37.88±6.19) mL/ (100 g·min), respectively. In the frontal lobe, mean aCBV, ATT and CBF values were (1.23±0.31) mL/100g, (1.55±0.15) s and (47.03±13.78) mL/(100 g·min), respectively. In the temporal lobe, mean aCBV, ATT and CBF values were (1.28±0.30) mL/100g, (1.54±0.12) s and (51.91±13.96) mL/(100 g·min), respectively. For the 17 ischemic cerebral hemispheres, mean aCBV, ATT and CBF values were (1.11±0.24) mL/100g, (1.46±0.35) s and (49.27±14.13) mL/(100 g·min) in the lesion peripheral region, (1.17±0.30) mL/100g, (1.51±0.37) s and (43.17±14.63) mL/(100 g·min) in the frontal lobe, and (1.21±0.35) mL/100g, (1.50±0.40) s and (49.25±20.85) mL/(100 g·min) in the temporal lobe. Compared with ischemic hemispheres, the hemorrhagic hemispheres showed significantly lower CBF in the peripheral region of the lesion (P<0.05). However, there's no statistical difference between two groups in term of aCBV and ATT. No evident statistical difference was seen in statistics of perfusion parameters of the frontal lobe and temporal lobe.Conclusions Hemorrhagic moyamoya disease has the lower perfusion than ischemic moyamoya. pCASL can detect the grade of blood flow failure in adults with hemorrhagic moyamoya disease, monitor tiny ischemic changes in peripheral frontal and temporal lobes, which can provide a basis for further research on early detection of rebleeding by monitoring hemodynamics.
[关键词] 烟雾病;伪连续动脉自旋标记成像技术;出血;血流动力学;磁共振成像
[Keywords] moyamoya disease;pseudo-continuous arterial spin labeling;hemorrhage;hemodynamics;magnetic resonance imaging

王宪雯 1, 2   吴芳 1   刘玥宏 3   王二玲 3   范文涛 3   张献昌 4   姚泽山 5   杨旗 3*  

1 首都医科大学附属宣武医院医学影像科,北京 100053

2 清华大学附属北京市垂杨柳医院放射科,北京 100022

3 首都医科大学附属北京朝阳医院医学影像科,北京 100020

4 西门子医疗磁共振科研合作部,北京 100000

5 安影科技(北京)有限公司,北京 100000

杨旗,E-mail:yangyangqiqi@gmail.com

全部作者均声明无利益冲突。


基金项目: 国家重点研发计划 2019YFC0120904 北京市自然科学基金资助项目 7191003
收稿日期:2021-06-26
接受日期:2021-11-25
中图分类号:R445.2  R543.4 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2022.01.002
本文引用格式:王宪雯, 吴芳, 刘玥宏, 等. 伪连续动脉自旋标记成像评估出血型烟雾病患者脑血流动力学研究[J]. 磁共振成像, 2022, 13(1): 6-10. DOI:10.12015/issn.1674-8034.2022.01.002

       烟雾病(moyamoya disease,MMD)是由于两侧颈内动脉末端、大脑前及中动脉起始端进行性狭窄、闭塞形成了各种易损侧支[1]、状如袅袅升腾的烟雾而得名。这个特征可能与出血有关,MMD患者发生脑卒中的概率为常人的7倍[2],其中出血型MMD以易损侧支血管断裂致颅内出血为主要表现,反复出血是出血型MMD的主要问题和最严重的不良事件,据报道每年有高达7%的再出血率[3]

       出血型MMD的随机对照试验检查结果表明,直接旁路术可以降低再出血发生率[3],选择恰当的手术时机、监测术后疗效、随访病例均需要对MMD患者进行准确的脑血流动力学评测。手术治疗仅需用于出现显著的临床症状或有依据表征脑灌注减低的患者[1]

       动脉自旋标记技术(arterial spin labeling,ASL)通过标识动脉血中的水分子,从而获得脑灌注方面的信息,伪连续动脉自旋标记技术(pseudo-continuous arterial spin labeling,pCASL)采用快速自旋回波序列,螺旋填充K空间,除了具备ASL技术相较传统灌注成像技术(PET、SPECT、动态磁敏感对比增强MRI等)免对比剂注射、经济便捷、无放射性、与传统灌注兼具较高的相关性等优点[4, 5]外,较其他ASL技术-连续式ASL(continuous ASL,CASL)、脉冲式ASL(pulsed ASL,PASL)等又具备信噪比更高、重复性更好等优点,成为目前ASL白皮书中推荐最多及临床采用较多的ASL技术[6]

1 资料与方法

1.1 纳入及排除标准

       (1)纳入标准:回顾性分析首都医科大学附属宣武医院2016年12月至2019年4月收治纳入研究的32例出血型或缺血型MMD患者,①患者通过DSA或MRA明确确诊为MMD,MMD诊断标准依照2012年日本MMD协会制定的诊断及治疗指南[1];② 18~65岁;③均在首发症状入院后3个月内接受pCASL检查。(2)排除标准:①存在pCASL检查禁忌证;②伴有可能导致颅内动脉狭窄、闭塞的疾病,如动脉粥样硬化、动脉炎等;③合并颅内肿瘤、颅脑外伤及其他神经系统疾病。

       本研究经首都医科大学伦理委员会批准,免除受试者知情同意,批准文号:临研审(2019) 076号。

1.2 pCASL检查

       磁共振扫描采用3.0 T MRI扫描仪(Magnetom Verio,Siemens healthcare,Erlangen),32通道头线圈。采用3D GRASE背景抑制pCASL,标记脉冲持续时间=1.5 s,4个PLD=1.5/2/2.5/3 s,无血流散相梯度,GRAPPA-2,重复时间=3.5/3.9/4.4/4.9 s,回波时间=22 ms,体素=3.4×3.4×5.0 mm3,层数=26层覆盖全脑,每个PLD采集12对标记像和控制像,总采集时间为6 min。M0图像:重复时间=6 s,PLD=4 s,采集时间为12 s。

1.3 图像处理

       pCASL图像在Matlab 2010a (MathWorks, Natick,MA)和SPM8 (Wellcome Department of Cognitive Neurology, UCL, London)软件上进行后处理及分析。pCASL图像进行运动校正,将每个PLD成对的标记像和控制像相减后平均,获得ΔM (i)图像,将pCASL图像与T1结构像配准,根据ASPECTS研究选取感兴趣区(region of interest,ROI)进行脑血流量(cerebral blood flow,CBF)、脑血容量(arterial cerebral blood volume,aCBV)及动脉通过时间(arterial transit time,ATT)的定量研究。每一ROI为横径10 mm、短径6 mm的椭圆形区域,在出血病例(图1)或梗死病例(图2)的病变层面分别于aCBV、ATT和CBF图像上选取3个ROI,依次为额叶1个(A1),颞叶1个(L1),出血或梗死周围区域1个(N1-避开病变显示区),在半卵圆中心层面分别于三幅灌注图像上选取2个ROI,依次为额叶1个(A2),颞叶1个(L2),同一病例同样标识ROI,三幅灌注图像位置一致。分别使用上述ROI对pCASL灌注图像进行区域CBF提取、aCBV和ATT值计算。计算公式1如下。

       其中ω (i)是PLD (=1.5/2/2.5/3 s)。

       每个PLD的CBF f i由公式2计算。

       其中R1a (=1.5 s-1或=0.61 s-1,1.5 T或3 T)是血液的纵向弛豫率,M0是脑组织的平衡磁化强度,α (=0.8)是标记效率,τ (=1.5 s)是标记脉冲的持续时间,λ (=0.9 g/mL)是血液/组织水分配系数。最终的CBF是每个PLD的估计CBF的平均值。

       最后,通过公式3,计算动脉aCBV。

图1  女,34岁,以右侧脑室出血为首发症状入院。A: T2WI示右侧脑室枕角及枕角旁含铁血黄素沉积;B: TOF示双侧颈内动脉颅内段狭窄,虹吸弯部以远双侧大脑前、中动脉闭塞;C: aCBV,出血层面血肿周围N1值1.27 mL/100g,出血及半卵圆中心层面额叶A1及A2平均值1.68 mL/100g,颞叶L1及L2平均值1.55 mL/100g;D: ATT,出血层面血肿周围N1值1.39 s,出血及半卵圆中心层面额叶A1及A2平均值1.50 s,颞叶L1及L2平均值1.33 s;E: CBF,出血层面血肿周围N1值55.35 mL/(100 g·min),出血及半卵圆中心层面额叶A1及A2平均值65.6 mL/(100 g·min),颞叶L1及L2平均值66.54 mL/(100 g·min)。
Fig. 1  A 34-year-old female patient with right intraventricular hemorrhage. A: T2WI shows hemosiderin with low signal intensity in the occipital horn of the right lateral ventricles and periventricular area; B: TOF detects stenosis of bilateral intracranial internal carotid arteries, and occlusion of bilateral siphon of internal carotid arteries, anterior and middle cerebral arteries; C: aCBV value around hematoma is 1.27 mL/100g. Average aCBV value of frontal lobe at the level of hemorrhage and centrum ovale is 1.68 mL/100g. Average aCBV value of temporal lobe is 1.55 mL/100g; D: ATT value around hematoma is 1.39 s. Average ATT value of frontal lobe at the level of hemorrhage and centrum ovale is 1.50 s. Average ATT value of temporal lobe is 1.33 s; E: CBF value around hematoma is 55.35 mL/(100 g·min). Average CBF value of frontal lobe at the level of hemorrhage and centrum ovale is 65.6 mL/(100 g·min). Average CBF value of temporal lobe is 66.54 mL/(100 g·min).
图2  男,26岁,以双侧大脑半球脑梗死入院。A: T2WI示双侧大脑半球多发脑梗死;B: TOF示双侧颈内动脉颅内段狭窄,虹吸弯部以远双侧大脑前、中动脉闭塞,左侧大脑后动脉闭塞,双侧颞部烟雾状血管形成;C: aCBV:梗死层面梗死周围N1值1.12 mL/100g,梗死及半卵圆中心层面额叶A1及A2平均值1.32 mL/100g,颞叶L1及L2平均值1.38 mL/100g;D: ATT:梗死层面梗死周围N1值1.57 s,梗死及半卵圆中心层面额叶A1及A2平均值1.58 s,颞叶L1及L2平均值1.69 s;E: CBF:梗死层面梗死周围N1值64.88 mL/(100 g·min),梗死及半卵圆中心层面额叶A1及A2平均值49.62 mL/(100 g·min),颞叶L1及L2平均值48.97 mL/(100 g·min)。
Fig 2.  A 26-year-old male patient with infarction of bilateral cerebral hemisphere. A: T2WI shows multiple infarcts of bilateral cerebral hemisphere; B: TOF detects stenosis of bilateral intracranial internal carotid arteries, and occlusion of bilateral siphon of internal carotid arteries, anterior and middle cerebral arteries, and left posterior cerebral artery; C: aCBV value around infarction is 1.12 mL/100g. Average aCBV value of frontal lobe at the level of infarction and centrum ovale is 1.32 mL/100g. Average aCBV value of temporal lobe is 1.38 mL/100g; D: ATT value around infarction is 1.57 s. Average ATT value of frontal lobe at the level of infarction and centrum ovale is 1.58 s. Average ATT value of temporal lobe is 1.69 s; E: CBF value around infarction is 64.88 mL/(100 g·min). Average CBF value of frontal lobe at the level of infarction and centrum ovale is 49.62 mL/(100 g·min). Average CBF value of temporal lobe is 48.97 mL/(100 g·min).

1.4 统计学方法

       本研究中出血型、缺血型各连续变量采用Shapiro-Wilk检验和正态Q-Q图验证数据分布的正态性。采用Levene′s方差齐性检验来验证方差齐的假设。正态且方差齐的连续变量两组间比较采用两独立样本t检验。非正态或方差不齐的连续变量采用Mann-Whitney U方法检验。上述统计学分析采用SPSS 24.0 (IBM,Armonk,New York,USA)进行,P<0.05代表差异有统计学意义。

2 结果

2.1 临床基线信息

       共计纳入32例出血型或缺血型MMD患者,统计出血半球21个,其中男6个,女15个,年龄(33.4±8.3)岁,缺血半球17个,其中男11个,女6个,年龄(32.5±5.3)岁。

       21个出血半球中右侧脑室出血7个,左侧脑室出血5个,蛛网膜下腔出血6个,基底节出血1个,额叶出血1个,颞叶出血1个。

2.2 出血组与梗死组的pCASL检查结果

       出血组与梗死组相比,病变周围区CBF值显著减低,差异有统计学意义(P<0.05),两组间aCBV及ATT差异不具有统计学意义,额叶及颞叶pCASL灌注差异不具有统计学意义(表1)。

表1  出血型与缺血型pCASL检查结果数值比较
Tab. 1  Comparison of pCASL test results between hemorrhagic and ischemia groups

3 讨论

3.1 技术可行性

       MMD的血管病理与其他脑血管疾病存在差异,其特点是迂曲纤细的侧支血管生成,导致对比剂(包括旋转标记的血液)通过缓慢,影响灌注图像的采集[7]。因此,在MMD中需要特殊的措施进行血流动力学评估。关于ASL作为临床工具评估脑血流动力学状态的研究已进行了多年[8, 9, 10],很多脑血管疾病的研究表明ASL可以作为评估成年MMD患者脑灌注的有效手段[11, 12, 13],而pCASL技术作为其中的佼佼者被广泛运用于临床[6]

3.2 临床意义

       MMD的卒中模式具有多样性,出血型患者相对非出血型病情更为凶险,患者多因颅内反复出血而死[14],出血型MMD自然过程(非手术)中随后的再出血事件与血流动力学衰竭显著相关,或者说血流动力学衰竭是出血型MMD继发出血的独立危险因素[15]。对于血流动力学受损的大脑半球,搭桥手术在预防继发性出血方面显示出显著的潜力,而对于血流动力学正常的大脑半球则没有显著的效果[15, 16]。因此,成人MMD患者出血后检测其血流动力学是否受损、监测何时受损可以为是否选择手术治疗、预防再出血提供有意义的信息。

3.3 结果分析

3.3.1 血流、血容的结果分析

       本次研究结果显示,以脑出血为首发症状的成人MMD患者病变区域较以梗死为首发症状的患者病变区域存在显著性血流减低,与郭翔等[17]、戚洲卿[18]研究结果相似,可能与血肿压迫或出血时所致的机械损伤有关,或者是出血侧狭窄或闭塞的血管造成该区域内缺血[12],血管的狭窄-闭塞会减少CBF,造成血流缓慢,血管反应性降低、烟雾血管形成等一系列代偿机制的变化,而由于侧支循环的建立,额叶、颞叶的血供可能为代偿期,这或许是出血与梗死半球额、颞叶部分灌注参数无明显差异的原因。

3.3.2 ATT的结果分析

       在临床中MMD脑血流动力学的病理过程通常被分为三期:在一期中患者的毛细血管灌注压(capillary perfusion pressure,CPP)、CBF及aCBV均处于正常水平;二期时受到脑组织侧循环代偿能力降低的影响CPP会呈现出降低,导致ATT升高,而CBF无明显影响;至三期(失代偿期)时动脉闭塞或狭窄会进一步发展,此时CPP降低更为显著,ATT继续升高,CBF也开始降低[19, 20]。本次研究中患者于首发症状3个月内行pCASL检查,故而猜测时间较短导致ATT无明显差异可能是二、三期病例较少的重要原因。

3.4 优点和不足

       从临床的角度来看,这个研究结果提示了pCASL上出血型MMD较缺血型存在更低灌注,通过pCASL技术可以无创性、可重复性观察脑内ROI灌注情况,提供脑内阳性征象周围有无因侧支循环建立而形成的脑血流动力改变依据。当然,本次研究存在一定的不足,首先,本文为横断面研究,初步探讨缺血和出血型MMD血流动力学差异,下一步需纵向随访研究探索pCASL在评估MMD出血风险的价值;其次,本研究的样本量相对较小,有导致结果偏倚的可能;再者,相关研究表明,脉络膜侧支血管是新生出血的预测因子[15,21],本次研究未加入侧支血管评测信息,因此后续研究中笔者期待扩大样本量、增加出血后纵向研究随访及侧支血管探讨,以期为此类患者的临床治疗提供更加详细、可靠的临床依据。

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