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综述
克罗恩病患者脑结构和功能改变的MRI研究进展
唐伍丽 李康

Cite this article as: Tang WL, Li K. Progress in MRI study of brain structure and functional alterations in patients with Crohn's disease[J]. Chin J Magn Reson Imaging, 2022, 13(8): 154-157.本文引用格式:唐伍丽, 李康. 克罗恩病患者脑结构和功能改变的MRI研究进展[J]. 磁共振成像, 2022, 13(8): 154-157. DOI:10.12015/issn.1674-8034.2022.08.035.


[摘要] 克罗恩病(Crohn's disease, CD)是一种病因不明的反复发作的炎症性肠病。越来越多的研究表明脑—肠轴在CD的发生发展中起着至关重要的作用,部分患者在临床上表现出焦虑、抑郁、心理障碍等症状;而长期焦虑、抑郁或处于高度心理压力下又可能导致疾病复发,因此,CD患者的心理精神状态在治疗过程中应该受到高度重视。目前,包含任务态、静息态的功能MRI已被广泛用于脑结构和功能方面的研究,并取得了一些有价值的成果。本文就CD患者脑结构和功能改变的MRI研究进展作一综述,为CD患者治疗策略的进一步优化提供神经影像学基础。
[Abstract] Crohn's disease (CD) is a kind of recurrent inflammatory bowel disease which has unknown etiology. A growing number of researches suggest that the brain-gut axis plays a critical role in the development of this disease, and some patients present clinical symptoms such as anxiety, depression, and psychological disorders. However, long-term anxiety, depression or high psychological stress may lead to the recurrence of the disease. Therefore, the psycho-psychiatric status of the patients should be high valued in the treatment process. Currently, functional magnetic resonance imaging, which includes task state and resting state, has been widely used to study structural and functional aspects of the brain, and some progress has been made. This article reviews the progress of MRI research on structural and functional brain alterations in patients with CD, so as to provide a neuroimaging basis for further optimizing the treatment strategies of these patients.
[关键词] 克罗恩病;功能磁共振成像;脑—肠轴;焦虑;抑郁
[Keywords] Crohn's disease;functional magnetic resonance imaging;brain-gut axis;anxiety;depression

唐伍丽 1, 2   李康 2*  

1 重庆医科大学,重庆 400016

2 重庆市人民医院放射科,重庆 401147

李康,E-mail:likangdoctor@126.com

作者利益冲突声明:全体作者均声明无利益冲突。


基金项目: 重庆市科技局科技创新与应用发展专项 cstc2020jscx-sbqwX0015 重庆市科卫联合项目 2019ZDXM008
收稿日期:2022-03-31
接受日期:2022-07-26
中图分类号:R445.2  R574 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2022.08.035
本文引用格式:唐伍丽, 李康. 克罗恩病患者脑结构和功能改变的MRI研究进展[J]. 磁共振成像, 2022, 13(8): 154-157. DOI:10.12015/issn.1674-8034.2022.08.035

       克罗恩病(Crohn's disease, CD)是一种病因不明的慢性进行性炎症性肠病(inflammatory bowel disease, IBD),可累及消化道任何部位[1]。其典型临床表现为腹痛、慢性腹泻、体质量减轻和疲劳[2]。研究表明,该病在西方国家发病率较高,如北美CD发病率为每10万人年0~20.2例,欧洲为每10万人年0.3~12.7例[3]。随着影响胃肠道的微生物群和表观遗传学的饮食及环境的西化,亚洲国家CD患病率正迅速上升[3, 4, 5, 6]。例如,在2001至2015年间,中国台湾地区该病的患病率从每10万人0.6例增加到了3.9例[7]。CD好发于30岁以下青年,需要及时并且长期维持治疗以预防疾病复发和肠道并发症[8]。CD的慢性进行性病程及复发和缓解交替的特点使患者的生活质量显著下降,同时也给患者带来了沉重的经济负担[9]。因此,CD的发病机制、诊断和治疗逐渐引起社会各界重视。

       功能磁共振成像(functional magnetic resonance imaging, fMRI)是指快速动态检测静脉血氧状态变化而引起MR信号产生微小差异的一种非侵入性的MRI技术[10]。fMRI分为任务态fMRI(task-state fMRI, t-fMRI)和静息态fMRI(resting-state fMRI, rs-fMRI)[11]。t-fMRI要求被试者执行如运动、语言、记忆、视觉等针对单一功能的特定任务;rs-fMRI则反映了无任务限制状态下的脑功能[12]。最近,fMRI已被广泛用于研究肠易激综合征、溃疡性结肠炎和CD患者的脑灰质结构变化[13]。且随着fMRI的日益普及,在与CD相关的神经成像研究中,患者脑部结构或功能异常的发现越来越多[14]

       研究表明,IBD患者出现焦虑、抑郁症状的风险增加,其中高达1/3和1/4的患者分别受到焦虑和抑郁症状影响,且CD患者比溃疡性结肠炎患者和健康对照组更易出现心理障碍症状[15, 16, 17]。据一项2000多名IBD患者的前瞻性研究显示,同时患有抑郁症的IBD患者临床复发时间明显缩短[18]。由于缓解期CD持续存在复发风险,导致患者心理压力较大,这种长期的不确定情况可能导致患者焦虑,而长期处于焦虑状态又可能促使疾病复发[19]。脑—肠轴是指人类肠道微生物群与中枢神经系统形成的双向通信途径[20]。越来越多的证据表明,肠道微生物群可以通过脑—肠轴调节大脑功能和相应的行为[21, 22]。临床活动性IBD患者异常的焦虑量表评分也为脑—肠轴的相互作用提供了有力证据[23]。此外,肠道微生物群变化也被广泛报道于中枢神经系统疾病中,例如阿尔茨海默病、自闭症、帕金森病等,进一步证明了大脑和肠道的相互作用[24]。脑—肠轴对CD患者胃肠道症状起着调节作用,而胃肠道症状的反复出现又可能引起患者精神心理状态改变,从而在患者脑结构或功能上表现出异常。因此,本文对CD患者脑结构和功能改变的MRI研究进展进行综述。

1 CD患者脑结构MRI

       基于体素的形态学测量利用高分辨率3D T1WI在体素水平上对脑组织密度和体积进行量化,是分析大脑结构功能的常用方法之一。在一项关于CD患者脑结构和功能的荟萃分析中显示,患者额叶内侧回的灰质体积(gray matter volume, GMV)减少[25]。Thomann等[26]使用联合独立分析也检测出IBD患者额中回和颞中回的GMV发生改变。最近的一项研究表明[14],CD患者左侧岛叶背侧前部和双侧岛叶后部的GMV减少;当把焦虑和抑郁作为协变量纳入分析后,左侧岛叶背侧前部的GMV差异不显著。在伴有焦虑症的肠易激综合征患者中也发现了相似的结果,包括额叶、岛叶等涉及情绪处理相关的脑区表现出GMV下降[27]。这说明这些脑区可能在CD患者情绪改变上发挥着重要作用。在伴或不伴腹痛的CD患者间也存在GMV差异,腹痛患者在岛叶、前扣带皮层、辅助运动区和背外侧前额叶皮质中表现出较低的GMV,且脑岛和前扣带皮层的GMV与患者腹痛严重程度之间的负相关关系表明这些结构可能参与内脏疼痛的处理[28]。此外,病程长短也会使患者的大脑结构发生相应改变。研究显示[29],右前扣带回、背内侧前额叶皮质、左侧岛叶的GMV以及左侧岛叶、眶额皮质的皮质厚度与病程呈负相关。这表明更长的病程将会导致多个脑区的GMV或皮质厚度减小,从而使得患者的认知、情绪、疼痛感受等发生相应改变。

       然而,在其他的一些关于IBD或CD患者脑功能的研究中,并未发现患者出现灰质结构上的变化,这可能是由于研究的样本量或研究中所选取的感兴趣区以及纳入标准的不同,所以导致各研究间得出的结果存在差异[30, 31, 32, 33]

2 CD患者的脑fMRI

2.1 t-fMRI

       t-fMRI要求受试者配合完成某项指定任务或给与受试者某种刺激,从而激发相应脑区功能改变。Nair等[34]使用一项言语流畅性任务来测试患者的认知功能。研究结果显示,患者双侧大脑半球激活更强,并且年轻CD患者与老年对照组之间的任务激活模式相似,这表明该病缓解期患者的认知功能可能表现出加速衰老的迹象。Agostini等[35, 36]使用Stroop任务发现CD患者内侧颞叶、脑岛、壳核和小脑的激活减少,而中扣带皮层的激活增加,且患者和对照组在静息状态时中扣带回的功能连接没有差异,因此表明两组中扣带回皮层活动的差异是由Stroop任务引起的,这说明该病活动期患者在应激适应方面与缓解期患者和对照组间存在差异。Gray等[37]通过内隐联想任务发现抗肿瘤坏死因子α治疗可降低IBD患者内脏敏感性,改善与杏仁核功能相关的认知情感偏差,由于循环中肿瘤坏死因子α的增加与患者胃肠道症状、抑郁或焦虑的程度有关,故该项研究发现抗肿瘤坏死因子α治疗可减轻CD患者的焦虑抑郁症状。此外,CD脑白质微观结构的相关研究显示,患者与语言功能相关的白质束出现显著变化,且其变化量与患者焦虑水平、病程长短具有相关性[38]。在上述CD患者脑t-fMRI的研究中均出现了不同脑区的异常激活,其中主要涉及认知情感和内脏敏感性相关脑区,这表明神经机制变化可能为患者认知和情感反应改变提供重要支持。

2.2 rs-fMRI

2.2.1 局部一致性及低频振幅分析

       局部一致性(regional homogeneity, ReHo)、低频振幅(amplitude of low frequency fluctuation, ALFF)分别描述了相邻体素区域活动步调的一致性和单个体素区域活动强度,两者均是描述静息态影像的重要特征。CD患者相关脑区ReHo改变与疾病活动程度、患者心理状态密切相关。例如,Huang等[13]研究发现活动期患者额上回内侧、额中回的ReHo值较健康对照组高,中央后回、辅助运动区、颞中回的ReHo值较低;而缓解期患者中央前、后回及壳核的ReHo值较低;此外,该项研究还发现患者部分脑区ReHo值改变与心理障碍评分具有相关性,如额中回ReHo值与患者的强迫、抑郁、偏执评分呈正相关。这表明CD患者脑功能状态与疾病活动程度有关,可能是由于活动期患者临床症状更明显,常需要住院治疗,生活质量更低,因此对患者的心理状态影响更大。

       CD患者ALFF相关研究显示,海马、前扣带回、岛叶、额上回和楔前叶等脑区的ALFF值较高[39]。而楔前叶、岛叶、扣带回等区域的ALFF改变是焦虑或抑郁症患者的特征性表现[40, 41]。因此,CD患者脑功能改变可能是其焦虑、抑郁症状发生率较健康人群高的重要原因之一。然而,Li等[42]针对CD患者静息态脑功能变化的研究结果显示,扣带回、额上回的ALFF变化虽与上述研究相同,但左侧海马区域相反,即ALFF值减低。这与活动性溃疡性结肠炎海马区ALFF变化一致[43]。由于海马区的功能主要涉及记忆储存和空间信息处理,且鲜有研究报道CD患者出现记忆力减退,故上述研究海马区ALFF变化不一致可能是受到了患者年龄或其他混杂因素的影响。

2.2.2 功能连接分析

       功能连接是描述不同脑区之间关系强弱的一种分析方法,其在CD患者脑功能分析中应用最为广泛。功能连接主要分为感兴趣区(region of interest, ROI)分析和独立成分分析(independent component analysis, ICA)。应用ROI分析方法,多项研究[14,32,42,44]报道了扣带回与包括中央后回、颞中回在内的多个脑区功能连接强度异常。扣带回是边缘系统的重要组成部分,尤其是前扣带回能协调多个大脑区域的信号,是操纵情绪行为和认知功能的枢纽[44]。因此,CD患者扣带回功能连接异常表明多个脑区协同作用参与患者的情绪处理与认知改变。

       对比ROI分析,算法较为复杂的ICA在CD患者脑功能连接分析中运用较少。由于ICA是对所有的血氧信号数据集进行分析,故不需要事先确定ROI。通过ICA发现,慢性腹痛可能会影响患者的脑功能连接。如Kornelsen等[31]的研究显示患者小脑、视觉和突显网络的功能连接改变;Li等[45]的研究结果同样显示患者的视觉和语言网络发生改变,CD患者长时间受到慢性腹痛的刺激,这可能是其视觉区域表现异常的原因。同时,在溃疡性结肠炎脑功能的相关研究中,也发现慢性肠道炎症和腹痛对大脑网络组织有持久的影响,即使肠道炎症已经减轻,这种影响也可能在溃疡性结肠炎患者的临床表现中发挥作用[46]。此外,病程长短也可能使患者的功能连接强度发生改变,如小脑和辅助运动区、额上回之间的连接强度与病程呈负相关,而小脑半球内和半球间的连接性与病程呈正相关[47, 48]

       ReHo、ALFF、功能连接均是rs-fMRI的重要分析方法,其中ReHo、ALFF反映局部脑区的功能变化,而功能连接研究不同脑区之间的相互作用,三者联合分析能够反映患者大脑网络变化的完整信息。上述静息态分析显示患者多个脑区功能改变,并且与患者的认知、情绪联系密切,这与任务态研究得出的结论相似,提示临床治疗CD时,不仅要关注肠道症状,还需重视患者的精神、心理状态。但目前的文献研究方法各异且研究结果涉及脑区众多,混杂因素干扰较大,因此有必要设计更加严密、周全的试验方案进一步验证。

3 总结与展望

       综上所述,CD患者多个脑区结构和功能发生改变,特别是扣带回、额叶、脑岛等与认知控制、情绪调节、疼痛处理的相关脑区,为该病的复发以及患者焦虑抑郁情绪的产生提供了神经影像学基础。以上几种fMRI研究方法相结合可以更好地评估患者大脑结构和内部神经网络的改变。虽然目前CD患者脑结构功能改变的相关研究较多,但多数研究结果不一致。这可能是由于大多数研究受到样本量的限制,且患者病程、有无腹痛、性别年龄比例、疾病亚型、免疫抑制剂的使用等均可能对大脑结构功能产生不同程度的影响。目前的研究大部分是对缓解期患者进行的横断面研究,无法确定大脑结构功能异常与疾病发生发展之间的潜在因果关系。因此,未来的研究应更多地倾向于纵向研究,将活动期与缓解期进行对比,同时扩大样本量以挖掘更多可靠的结果,为CD患者治疗策略的优化提供更加可靠的依据。

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