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基础研究
轻度认知障碍患者言语流畅性下降的静息态功能磁共振研究
郭春蕾 何家恺 马跃 孙继飞 张斌龙 王智 洪洋 张磊 方继良 罗萍

Cite this article as: Guo CL, He JK, Ma Y, et al. A resting-state fMRI study on the verbal fluency decline in mild cognitive impairment[J]. Chin J Magn Reson Imaging, 2022, 13(8): 60-64, 74.本文引用格式:郭春蕾, 何家恺, 马跃, 等. 轻度认知障碍患者言语流畅性下降的静息态功能磁共振研究[J]. 磁共振成像, 2022, 13(8): 60-64, 74. DOI:10.12015/issn.1674-8034.2022.08.011.


[摘要] 目的 采用低频振幅(amplitude of low frequency fluctuation, ALFF)初步探索轻度认知障碍(mild cognitive impairment, MCI)患者言语流畅性下降的脑机制。材料与方法 前瞻性纳入20例MCI患者(MCI组)及16 例性别、年龄、受教育程度相匹配的健康人作为对照组(健康对照组),入组前分别采集两组临床资料、神经心理学量表和静息态功能磁共振(resting-state functional magnetic resonance, rs-fMRI)数据。采取ALFF分析方法,比较MCI组与健康对照组静息态脑功能差异,并进一步采用Spearman相关分析分别观察ALFF变化的脑区与言语流畅性测试量表的相关性。结果 与健康对照组比较,MCI 组患者右侧岛叶/颞上回ALFF降低(高斯随机场校正,voxel P<0.005,cluster P<0.05)。未发现ALFF升高脑区。降低的ALFF值与蒙特利尔认知量表基础版的流畅性测试有显著的正相关性(rs=0.500,P=0.025)。结论 MCI存在右侧岛叶/颞上回大脑活动降低,可能是患者言语流畅性下降的原因。
[Abstract] Objective Amplitude of low frequency fluctuation (ALFF) was used to preliminarily explore the brain mechanism of verbal fluency decline in patients with mild cognitive impairment (MCI).Materials and Methods A total of 20 MCI patients (MCI group) and 16 healthy controls (healthy controls group) matched in gender, age and education level were recruited prospectively. Before enrollment, clinical data, neuropsychological scales and resting-state functional magnetic resonance imaging data were collected. ALFF was used to compare the differences of resting-state brain function between MCI group and healthy controls group, and the Spearman correlation between the change brain regions of ALFF and verbal fluency scales was further observed.Results Compared with the healthy control group, the ALFF of the right insula/superior temporal gyrus was decreased in MCI group (Gaussian random field correction, voxel P<0.005, cluster P<0.05). No ALFF elevation was found in brain regions. There was a significant positive correlation between reduced ALFF and fluency test of Montreal cognitive assessment-basic(rs=0.500, P=0.025).Conclusions MCI has decreased brain activity in the right insula/superior temporal gyrus, which may be underlying the mechanism of patient's verbal fluency decline.
[关键词] 轻度认知障碍;静息态功能磁共振成像;低频振幅;言语流畅性下降;岛叶;颞上回
[Keywords] mild cognitive impairment;resting state functional magnetic resonance imaging;low frequency amplitude;verbal fluency decline;insula;superior temporal gyrus

郭春蕾 1   何家恺 2   马跃 1   孙继飞 1   张斌龙 3   王智 1   洪洋 4   张磊 4   方继良 1*   罗萍 4*  

1 中国中医科学院广安门医院功能成像研究室,北京 100053

2 中国中医科学院针灸研究所机能室,北京 100700

3 中国中医科学院广安门医院针灸科,北京 100053

4 中国中医科学院广安门医院放射科,北京 100053

罗萍,E-mail:luoping76@163.com 方继良,E-mail:fangmgh@163.com

作者利益冲突声明:全部作者均声明无利益冲突。


基金项目: 北京市自然科学基金面上项目 7212191 中国中医科学院科技创新工程 CI2021A03316
收稿日期:2022-04-27
接受日期:2022-08-01
中图分类号:R445.2  R749.1 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2022.08.011
本文引用格式:郭春蕾, 何家恺, 马跃, 等. 轻度认知障碍患者言语流畅性下降的静息态功能磁共振研究[J]. 磁共振成像, 2022, 13(8): 60-64, 74. DOI:10.12015/issn.1674-8034.2022.08.011

       轻度认知障碍(mild cognitive impairment, MCI)是未达到痴呆状态,且日常生活功能未受损或轻度受损的认知功能减退性疾病。目前认为,MCI与多种痴呆有关,特别是与阿尔茨海默病(Alzheimer's disease, AD)关系密切。据流行病学调查显示,我国MCI患病率高达19%,且患病率逐年增长[1]。部分MCI患者可能会随着时间推移逆转为认知正常状态[2, 3, 4],给诊断带来了巨大挑战。但其诊断标准不一,客观量表的敏感性不足,脑功能异常模式尚不清楚,以上因素制约了MCI的治疗和药物研发。

       研究发现,言语流畅性下降对诊断和区分MCI与其他疾病有重要意义,但未从影像学的角度探究言语流畅性下降与脑区功能异常的关系,未阐明其机制[5, 6, 7]。近年来,静息态功能磁共振成像(resting-state functional magnetic resonance imaging, rs-fMRI)技术广泛应用于多种神经精神疾病的研究,可在活体状态下对大脑功能进行可视化,已被证实为一种安全可靠的研究手段[8]。低频振幅(amplitude of low frequency fluctuation, ALFF)反映了大脑局部区域自发脑活动情况,已在MCI研究中得到应用[9, 10]。然而,研究MCI言语流畅性下降脑机制的fMRI研究较少。因此,本研究基于ALFF分析方法,分析MCI言语流畅性下降的脑机制,为临床靶向治疗提供一定依据。

1 材料与方法

1.1 研究对象

       参照影像学样本量的文献以及既往MCI相关机制研究文献[11, 12, 13],本研究从2021年7月到2022年3月,前瞻性纳入20例来自广告招募及北京慈爱嘉养老服务有限公司负责管理的50家社区居家养老服务中心的MCI患者(MCI组)。研究采用2004年Jak/Bodi的诊断标准[14],该标准较传统的Petersen诊断标准敏感度和特异度更高,诊断假阳性率更低,可提高MCI诊断的准确性[14, 15]。MCI组纳入标准:(1)有明显认知下降,但日常生活功能基本正常,日常生活功能采用社会活动功能量表(Functional Activities Questionnaire, FAQ)进行评估,总分30分,分值>9分提示存在日常生活活动功能障碍;(2)年龄55~79岁,汉族,右利手;(3)蒙特利尔认知量表基础版(Montreal Cognitive Assessment-Basic, MoCA-B)评分低于以下标准者:受教育年限≤6年,评分≤19分;7~12年,评分≤22分;>12年,评分≤24分;(4)磁共振检查未见明显脑实质病变。患者排除标准:(1)各种原因导致的痴呆;(2)炎症脑血管病、脑炎、脑肿瘤、脑外伤、癫痫、帕金森病等其他导致认知下降的神经系统疾病;(3)严重的精神疾病,如重度抑郁等,17项汉密尔顿抑郁量表(17-item Hamilton Depression Scale, HAMD-17)>7分,汉密尔顿焦虑量表(Hamilton Anxiety Scale, HAMA)>7分;(4)患有急性或严重威胁生命的疾病,有心脏起搏器、金属关节、幽闭恐惧症等磁共振检查禁忌证;(5)严重的视力、听力或语言问题不能配合认知量表评估;(6)服用精神类药物或药物滥用。

       同时,招募同样来源的16例性别、年龄、受教育程度相匹配的健康人作为对照(健康对照组)。健康对照组纳入标准:(1)无明显记忆下降或认知障碍主诉;(2)无神经精神疾病病史。健康对照组排除标准:(1)有磁共振检查禁忌证(心脏起搏器、金属关节、幽闭恐惧症等);(2)磁共振检查见明显脑器质性病变。MCI组和健康对照组均在入组前先进行HAMD-17和HAMA评估精神状态,再进行华山版听觉词语学习测验(Auditory Verbal Learning Test-Huashan version, AVLT-H)、形状连线测验A和B(Shape Trails Test A&B, STT A&B)、动物词语流畅性(Animal Fluency Test, AFT)及波士顿命名测试(Boston Naming Test, BNT)以及FAQ评估。AVLT-H、STT A& B、AFT、BNT以及FAQ分别评估记忆、执行、语言功能和日常生活功能,至少同一个认知域(记忆、语言、执行功能)中的2个神经心理检查测试损害程度均大于1.0 SD(经年龄校正的常模)、每一个认知域(记忆、语言、执行功能)中有1个神经心理检查测试损害程度均大于1.0 SD(经年龄校正的常模)或者FAQ评分为9分,可认为存在认知障碍。患者单独进行MoCA-B评估。本试验获得中国中医科学院广安门医院伦理委员会批准(批准文号:2021-077-KY-01),全体受试者均签署了知情同意书。

1.2 rs-fMRI数据采集

       所有被试均在中国中医科学院广安门医院放射科进行rs-fMRI扫描,设备为德国西门子Magneton Skyra 3.0 T磁共振,采用标准20通道头颈联合线圈。扫描过程中嘱被试保持安静、闭眼、放松状态。先进行T2WI MRI平扫,以排除严重脑器质性病变,如脑梗死、脑缺血等。再进行3D T1WI脑结构像扫描,扫描参数为:重复时间(repetition time, TR)2530 ms,回波时间(echo time, TE)2.98 ms,视野(field of view, FOV)256 mm×256 mm,层厚1.0 mm,层间距1.0 mm,层数128层,矩阵256×192,翻转角(flip angle, FA)7°;最后进行血氧水平依赖(blood oxygenation level dependent, BOLD)的静息态功能扫描,参数为:TR 2000 ms,TE 30 ms,层厚3.5 mm,层间隔0.6 mm,层数32 层,FOV 224 mm×224 mm,矩阵64×64,FA 90°。每个被试各扫描一次fMRI,扫描序列、扫描参数保持一致。

1.3 rs-fMRI数据预处理

       所有rs-fMRI原始数据均采用基于MATLAB(R2020a)平台的DPABI 6.0进行处理。预处理首先对原始DICOM数据进行格式转换,先剔除前10个时间点的数据,再进行时间层校正、头动校正(排除所有平动方向移动>3 mm和转动方向>3°)的数据,所有被试头动均合格,接着回归白质信号、脑脊液信号等噪声协变量、去线性漂移,采用统一分割算法进行空间标准化得到每个被试在MNI标准空间的功能像,然后将空间标准化后的功能像重采样到3 mm×3 mm×3 mm体素大小,选择半高宽值为4 mm的高斯平滑核进行空间平滑提高信噪比,最后将得到的数据在0.01~0.1 Hz频段进行滤波。

1.4 ALFF分析

       计算ALFF指标并进行Z值标准化,随后将两组标准化后的数据进行两样本t检验,将年龄,受教育年限以及头动参数值作为协变量回归。参考rs-fMRI研究的阈值[16, 17],采用高斯随机场(Gaussian Random Field, GRF)校正,设定对比差异voxel P<0.005,cluster P<0.05为差异具有统计学意义,最后将结果进行提值并进行可视化展现。计算、统计和结果呈现均采用DPABI 6.0。

1.5 临床数据分析

       采用SPSS 26.0软件统计分析数据。计数资料采用卡方检验。计量资料符合正态分布用均数±标准差(x¯±s)表示;不符合正态性分布或部分不符合正态分布则采用秩和检验,用中位数(四分位数间距)[M(IQR)]表示。P<0.05表示差异有统计学意义。两组ALFF两样本t检验的阳性结果提值后得到的ALFF值分别与MCI组MoCA-B的流畅性测试、AFT、BNT量表进行相关性分析,两组均服从正态分布用Pearson相关分析,否则用Spearman相关分析,P<0.05表示差异有统计学意义。

2 结果

2.1 人口学特征

       MCI组和健康对照组在性别、年龄、教育年限和平均FD-Jenkinson上的差异无统计学意义;两组的FAQ、HAMD-17以及HAMA均在正常范围;经过受教育年限的调整,患者组的MoCA-B均未达到正常水平;AVLT-H(N5)、AVLT-H(N7)、STT A、STT B、AFT、BNT量表得分上差异有统计学意义(表1表2)。

表1  人口学资料
Tab. 1  Demographic data
表2  MCI组MoCA-B各个认知域测试完成情况
Tab. 2  The completion of each cognitive domain test of MOCA-B in MCI group

2.2 图像数据两样本t检验结果

       与健康对照组相比,MCI组右侧岛叶/颞上回ALFF降低(GRF校正,voxel P<0.005,cluster P<0.05),未见ALFF升高的脑区(表3图1)。

图1  MCI组与健康对照组两样本t检验显著的脑区和两组对比图。1A中蓝色团块表示与健康对照组相比,MCI组ALFF降低的脑区(右侧岛叶/颞上回),色条代表t值;1B表示MCI组和健康对照组ALFF值的差异,****表示P<0.0001。MCI:轻度认知障碍;ALFF:低频振幅。
Fig. 1  Significant brain regions of two sample t test in MCI group and healthy controls group and comparison of the two groups. The blue mass in 1A represents the brain region (right insula/superior temporal gyrus) with decreased ALFF in MCI group compared with healthy control group, color bar represents t value. 1B represents the difference in ALFF values between the MCI group and the healthy control group, and **** represents P<0.0001. MCI: mild cognitive impairment; ALFF: amplitude of low frequency fluctuation.
表3  MCI组与健康对照组两样本t检验显著的脑区
Tab. 3  Significant brain regions of two sample t test in MCI group and healthy controls group

2.3 相关性分析结果

       Spearman相关分析结果显示,MCI组降低的ALFF值与MoCA-B中的流畅性测试显著相关(rs=0.500,P=0.025),但与AFT和BNT无显著相关(图2)。

图2  MoCA-B流畅性测试图。MoCA-B中流畅性测试的个数与MCI组ALFF值的相关,二者呈正相关(rs=0.500,P=0.025)。MoCA-B:蒙特利尔认知评估量表基础版;MCI:轻度认知障碍;ALFF:低频振幅。
Fig. 2  Moca-B fluency test chart. The number of fluency tests in MOCA-B was positively correlated with the ALFF value of MCI group (RS=0.500, P=0.025). MoCA-B: Montreal Cognitive Assessment-Basic; MCI: mild cognitive impairment; ALFF: Amplitude of low frequency fluctuation.

3 讨论

       本研究是首个采用Jak/Bondi诊断标准,以AVLT-H、STT A&B、AFT、BNT评估多个认知域以及FAQ评估日常生活功能来筛查MCI患者,同时结合MoCA-B和rs-fMRI技术研究MCI言语流畅性下降的脑机制研究。本研究发现在静息态状态下MCI存在局部脑功能异常改变:与健康对照相比,MCI患者局部脑功能活动降低,表现为右侧岛叶和右侧颞上回ALFF值降低,且与MoCA-B中的流畅性测试显著相关。

3.1 岛叶与语言和注意力

       语言是人类特有的一种认知能力,在其他疾病上可观察到注意力受损与言语流畅性有一定联系[18]。注意力受损是MCI患者的常见症状[19],且注意力一定程度上影响记忆力[20],记忆减退是MCI的主要临床表现。岛叶作为突显网络的核心节点,是参与外部导向和内部导向注意或与自我相关认知等其他大型脑网络之间的动态切换的中枢[21]。突显网络、默认网络、执行控制网络功能异常是MCI的常见改变,且与AD的疾病进程和AD前期诊断相关[22, 23]。岛叶还与语言产生和处理有关[24, 25],岛叶功能异常可能提示言语记忆功能受损[26]

       Bi等[26]提出的一种基于rs-fMRI数据和遗传数据的遗传进化随机森林算法,发现岛叶、额上回、杏仁核等脑区是早期MCI相关的致病脑区。Duan等[27]发现,MCI患者的岛叶、右侧颞顶区和右侧额下区局部脑血流较健康人降低。樊响等[28]表明,与健康人比较,MCI患者左侧岛叶、左侧壳核、双侧尾状核和双侧海马旁回ALFF降低。此外,赵澄等[29]发现,MCI患者右侧岛叶前部-额叶岛盖与左侧嗅皮质、左侧顶上小叶功能连接较健康人显著降低,左侧岛叶前部-额叶岛盖与嗅皮质的功能连接减低。Hu等[30]表明,MCI患者双侧岛叶和右侧小脑的度中心性降低。本研究的结果也发现了岛叶功能活动下降,可能与患者的言语流畅性下降有关。

3.2 颞上回与听力和言语功能

       颞上回位于顶叶、枕叶和颞叶交汇处,是听觉言语中枢[31, 32]。MCI的神经心理学改变包括语言功能减退[33],此外,听力受损与认知下降存在明显相关,严重的听力下降与更高的痴呆发病率相关[34, 35]。颞上回位于默认网络,默认网络参与注意力集中和多种形式的复杂认知活动,与记忆或抽象思维有关[36, 37]。在MCI早期,默认网络功能即出现自发活动增强,为功能代偿的一种形式[38]

       既往研究表明,MCI患者多个脑区,包括颞叶、顶叶区存在低灌注和低代谢[39]。此外,fMRI研究也发现MCI患者颞上回的局部脑活动下降,颞上回与其他脑区的功能连接下降。汪腾龙等[40]发现,MCI患者右侧颞上回、右侧颞中回、颞极、中央后回的局部一致性比健康人降低,后扣带回/楔前叶与左侧颞上回、左侧颞中回、左侧角回、左侧枕中回功能连接降低。另外,吴钦娟等[41]发现,MCI患者后扣带与右侧颞上回、双侧颞中回、双侧舌回功能连接显著降低。Fam等[42]表明,MCI患者左侧颞上回、岛叶和右侧扣带回较健康人的时间全局效率要低。MCI患者右侧颞上回ALFF降低可能是患者言语流畅性下降的表现,这在MoCA-B的流畅性测试也有体现。

       MCI脑功能研究的Meta分析研究结果表明,MCI患者存在多个脑区的ALFF降低,包括双侧岛叶、左侧颞枕区、双侧后扣带/楔前叶等[43, 44]。此外,MCI脑结构研究的meta分析也发现,岛叶和颞上回体积共同减少是MCI的危险因素,可能反映了沟通障碍、精神或社会活动刺激减少[45]。我们的结果有类似发现,再次验证了MCI存在岛叶和颞上回局部脑功能异常,岛叶和颞上回的功能改变在MCI病程中是常见的,而且这种改变可能是MCI患者言语流畅性下降的原因之一。但是,也有研究发现MCI患者存在岛叶和颞叶ALFF升高[46, 47],认为与疾病早期出现的脑功能代偿、伴随疾病或MCI的亚型相关。

3.3 局限性

       本研究尚存在许多不足:第一,纳入的样本量较小,未对MCI进行分型;第二,本研究关注的指标较少。考虑到本研究纳入患者的标准较严格,假阳性的可能性较低。基于上述的原因,患者和健康对照差异脑区较少的原因可能是样本量较小。未来将在更大样本量的基础上,对MCI的亚型进行研究,进一步探索MCI患者言语流畅性下降发生的脑机制,验证是否是由于岛叶和颞上回功能异常或者其他与言语相关的脑区功能异常导致的。此外,鉴于前期研究发现岛叶和颞上回体积减小与MCI的功能改变有关,我们未来的研究也将结合基于体素的形态学方法,经过灰质体积校正后再次验证MCI存在功能异常的脑区。

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