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综述
抗N-甲基-D-天冬氨酸受体脑炎的磁共振成像研究进展
刘涵静 罗天友

Cite this article as: Liu HJ, Luo TY. Research progress in MRI of anti-N-methyl-D-aspartate receptor encephalitis[J]. Chin J Magn Reson Imaging, 2022, 13(9): 139-143.本文引用格式:刘涵静, 罗天友. 抗N-甲基-D-天冬氨酸受体脑炎的磁共振成像研究进展[J]. 磁共振成像, 2022, 13(9): 139-143. DOI:10.12015/issn.1674-8034.2022.09.033.


[摘要] 抗N-甲基-D-天冬氨酸受体(N-methyl-D-aspartate receptor, NMDAR)脑炎是自身免疫性脑炎中最常见的一种类型,其发病率逐年上升,有多种因素可触发抗NMDAR脑炎的发生,并可分为伴肿瘤型与不伴肿瘤型。抗NMDAR脑炎临床表现复杂多样,诊断困难。近半数患者首次常规MRI有异常表现,而高级 MRI是加深对该病影像及病理和病理生理学认识的有效补充。本文对近年来抗NMDAR脑炎常规MRI及高级MRI技术研究新进展进行综述,旨在提高对该病的认识。
[Abstract] Anti-N-methyl-D-aspartate receptor (NMDAR) encephalitis is the most common type of autoimmune encephalitis, and its incidence is increasing year by year. There are many factors that can trigger the occurrence of anti-NMDAR encephalitis, which can be divided into neoplastic and non-neoplastic types. The clinical manifestations of anti-NMDAR encephalitis are complex and varied, and it is difficult to be diagnosed. Nearly half of the patients showed abnormal signals on conventional MRI for the first time, and advanced MRI is an effective supplement to deepen the understanding of imaging and pathology and pathophysiology of the disease. In this paper, the recent advances in conventional MRI and advanced MRI technology of anti-NMDAR encephalitis were reviewed, in order to improve the understanding of the disease.
[关键词] 抗N-甲基-D-天冬氨酸受体脑炎;脑炎;磁共振成像
[Keywords] anti-N-methyl-D-aspartate receptor encephalitis;encephalitis;magnetic resonance imaging

刘涵静    罗天友 *  

重庆医科大学附属第一医院放射科,重庆 400016

*罗天友,E-mail:ltychy@sina.com

作者利益冲突声明:全体作者均声明无利益冲突。


收稿日期:2022-05-06
接受日期:2022-09-07
中图分类号:R445.2  R512.3 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2022.09.033
本文引用格式:刘涵静, 罗天友. 抗N-甲基-D-天冬氨酸受体脑炎的磁共振成像研究进展[J]. 磁共振成像, 2022, 13(9): 139-143. DOI:10.12015/issn.1674-8034.2022.09.033

       抗N-甲基-D-天冬氨酸受体(N-methyl-D-aspartate receptor, NMDAR)脑炎是自身免疫性脑炎(autoimmune encephalitis, AE)最常见的一种类型。该病起病急,临床症状重,近半数患者首次常规MRI有异常信号表现。不少研究认为,高级MRI是对该病影像学表现及病理和病理生理学认识的有效补充,可为其诊断及预后评估提供有效帮助。本文对近年来抗NMDAR脑炎MRI研究进展作一综述,旨在提高对该病的认识。

1 临床概述

       抗NMDAR脑炎为最常见的AE,约占所有AE的80%[1]。该病多见于儿童、青年,女性多于男性,目前全球报道的抗NMDAR脑炎发病率明显上升,在青年人中其发病率甚至超过了病毒性脑炎(viral encephalitis, VE)[2, 3, 4]。研究发现有多种因素可触发抗NMDAR脑炎的发生,并可分为伴肿瘤型与不伴肿瘤型。约25%的患者伴发肿瘤,这些肿瘤可以是卵巢畸胎瘤、小细胞肺癌、霍奇金淋巴瘤、慢性粒细胞白血病和子宫腺癌等[5, 6, 7, 8],其中卵巢畸胎瘤是抗NMDAR脑炎最常伴发的肿瘤,以成熟畸胎瘤多见[9, 10]。不伴肿瘤型可见于病毒和寄生虫感染,也可见于炎性脱髓鞘患者,其中以单纯疱疹病毒感染与其关系最密切[11, 12, 13, 14, 15]。此外,近期有文献[16, 17]报道COVID-19感染合并抗NMDAR脑炎的病例。

       抗NMDAR脑炎临床表现复杂多样,缺乏特异性,疾病过程大致可分为前驱期、精神症状期、反应迟钝期、多动期和恢复期五个不同阶段。一般认为[18, 19, 20],前驱期通常以非特异性流感样症状为特征;精神症状期可出现冷漠、焦虑、易怒、抑郁和恐惧等情绪改变;反应迟钝期和多动期可交替出现,反应迟钝期常表现为缄默和反应迟钝,多动期主要表现为自主神经功能障碍和异常运动;恢复期是一个缓慢的过程,恢复的顺序常与症状出现的顺序相反。约75%的患者可康复或仅遗留轻微后遗症,另外25%的患者将会遗留严重残疾甚至死亡[19]。抗NMDAR脑炎的确诊依赖于在患者脑脊液或血清中检出相应自身抗体。

2 常规MRI

       抗NMDAR脑炎的临床表现缺乏特异性,确诊依赖于抗体检测,但其检测费用高、耗时长、不易普及。T1加权成像(T1 weighted imaging, T1WI)、T2加权成像(T2 weighted imaging, T2WI)、T2加权液体衰减反转恢复(fluid-attenuated inversion recovery, FLAIR)序列和增强扫描T1WI等常规MRI[21]对该病的早期诊断和预后评估有一定作用。

       据报道[22, 23, 24],约23%~50%的抗NMDAR脑炎患者首次常规MRI检查颅内可见异常表现,异常信号可累及边缘系统、大脑白质和灰质、小脑以及脑干,以海马、额叶及颞叶多见。部分患者表现为脑内散在异常信号,当边缘系统受累时,病灶可对称分布,而当白质或深部灰质受累为主时,病灶多不对称,常呈斑片状[25, 26]。部分患者以灰质受累为主,表现为局灶性皮质异常信号,相应脑回肿胀,邻近脑沟变窄[27]。个别病例可存在侧脑室颞角扩大、垂体病变等[23]

       抗NMDAR脑炎脑实质病灶在T1WI上表现多不显著,可呈等、稍低或低信号;T2WI上呈稍高或高信号;T2 FLAIR序列病灶显示最佳,常呈稍高或高信号[23]。增强扫描T1WI上,部分病灶可呈“脑回状”或斑片状强化,部分病灶强化不明显,当累及脑膜时可表现为局部脑膜增厚或脑沟内小血管影增多[26, 27]。有文献[28]报道抗NMDAR脑炎的非典型病灶,如1例被误诊为韦尼克脑病的男性患者双侧额叶皮质见条带状对称性高信号及胼胝体压部见对称性“彩虹样”高信号,邻近脑回未见明显肿胀;另1例患者双侧基底节区见对称性斑片状高信号,其MRI表现与肝豆状核变性相似。

       抗NMDAR脑炎常规MRI表现往往难以与AE的其他类型进行鉴别,有研究发现脑膜强化在抗NMDAR脑炎患者中更为常见,可作为急性期抗NMDAR脑炎与电压门控钾通道复合体抗体脑炎的鉴别点[29]。抗NMDAR脑炎常表现为弥漫性脑炎,而抗γ-氨基丁酸B型受体脑炎及抗富亮氨酸胶质瘤失活1蛋白脑炎以边缘叶受累为主[30]。抗NMDAR脑炎与VE的发病方式、临床表现都很相似,但二者的治疗方式和预后都不尽相同[31],常规MRI对早期鉴别诊断有一定价值。当病灶累及边缘系统时,AE与VE病灶分布差异较明显,AE病灶常呈对称性分布,VE病灶常呈不对称性分布[25]。总之,常规MRI为诊断AE各亚型和与VE患者的鉴别诊断提供了有效的线索,对指导临床治疗有一定的意义。

       常规MRI表现异常与抗NMDAR脑炎患者的预后不良及复发相关。Lei等[32]发现常规MRI表现异常患者较常规MRI表现正常患者的简易智能检查量表评分更低,表明常规MRI表现异常患者认知功能受损更严重;Balu等[33]发现MRI表现异常是抗NMDAR脑炎预后不良的独立预测因子,并将此项纳入他们构建的诊断抗NMDAR脑炎1年后神经功能预测评估表中。Zhang等[22]发现海马受累患者随访期间改良Rankin评分明显高于海马未受累患者,认为海马受累是抗NMDAR脑炎患者预后不良的重要预测因素;Feng等[34]应用生存分析发现颅内MRI病灶≥3个或脑干受累的抗NMDAR脑炎患者复发风险更大。

       尽管仅有部分病例显示异常表现,常规MRI对抗NMDAR脑炎的诊断及预后评估仍有一定价值。当患者存在精神行为异常、癫痫发作、近事记忆障碍等神经精神症状,MRI平扫显示脑内散在非特异性异常信号,增强扫描T1WI上病灶无强化或呈“脑回状”、斑片状强化,或出现脑膜增厚、脑沟内小血管影增多等表现时,应考虑到抗NMDAR脑炎的可能性。当常规MRI显示病灶个数较多或海马、脑干受累,应加强患者管理,以有利于改善患者预后。

3 高级MRI

3.1 结构成像

       结构成像简单易行,被广泛应用于探测多种神经精神疾病较为隐匿的脑微结构变化。形态学分析和容积分析作为常见的结构成像方法,可进一步揭示抗NMDAR脑炎患者脑体积减小情况及其与认知的关系。Gomeze等[35]在一项纵向研究中应用自动脑区分割法对25例抗NMDAR脑炎患者进行脑体积分析,发现患者脑总体积、小脑体积、脑干体积明显减小。Xu等[36]对24例急性期后抗NMDAR脑炎患者进行基于表面的形态学分析以及海马分割研究,发现患者语言网络、默认网络的相关脑区及左侧海马角的灰质体积减小,而且这些改变与脑炎长期后遗症引起的认知功能障碍有关。Bartels等[37]对38例儿童抗NMDAR脑炎患者进行容积MRI分析,发现随着时间推移,有抗NMDAR脑炎病史的儿童患者表现出显著的脑容量损失及皮层和皮层下灰质减少所致的低于年龄预期的大脑发育异常。因此,当患者在随访过程中出现脑萎缩,提示更应关注患者认知功能受损情况。由于结构成像结果较为单一,常联合应用其他功能成像方法以全面揭示抗NMDAR脑炎的结构与功能改变。

3.2 扩散成像

       扩散加权成像(diffusion weighted imaging, DWI)能检测组织中水分子扩散运动受限的方向和程度,由于其敏感性高、扫描时间短,是临床上最常使用的头颅MRI功能成像序列。抗NMDAR脑炎大部分病灶DWI显示为轻度扩散受限或扩散无明显受限,多以稍高或等信号表现为主,部分病例局部脑回可呈高信号,表现为“皮质绸带征”[27,38]。但由于穿透效应的影响,可能导致图像出现假阳性表现。DWI上抗NMDAR脑炎信号改变缺乏量化标准,其表观扩散系数值的价值有待今后进一步探讨。

       扩散张量成像(diffusion tensor imaging, DTI)由DWI发展而来,能进一步量化水分子扩散运动中的各向异性,是评估脑白质结构变化的MRI技术。Phillips等[39]对46例抗NMDAR脑炎患者进行DTI研究,发现患者存在广泛的皮层下白质损伤,且这类损伤与患者持续性认知障碍相关。Liang等[40]利用DTI基于体素的分析和多变量模式分析也得出相似的结论,他们发现抗NMDAR脑炎患者右侧颞中回、左侧小脑中脚、右侧楔前叶各向异性分数减低,左侧颞中回和左侧额叶平均扩散率升高,且这些改变与患者认知障碍相关。但DTI的原理是基于水分子服从高斯分布的假设[41],由于组织中细胞膜、神经元和其他细胞器的存在,水分子的实际扩散服从非高斯分布,因此DTI的扩散参数不能准确描述水分子的扩散,尤其是富含神经元细胞和树突的灰质中的水分子的扩散。未来可采用更高阶的扩散成像技术进一步探讨抗NMDAR脑炎患者脑灰质的结构变化,如扩散峰度成像[42]和神经突起方向离散度与密度成像[43]

3.3 灌注成像

       灌注成像通常采用动脉自旋标记成像(arterial spin labeling, ASL)技术。ASL技术简便,且可避免血脑屏障给示踪剂带来的阻滞作用,通过直接示踪动脉血水分子运动以显示脑血流灌注情况,从而提高了脑血流量(cerebral blood flow, CBF)测量的准确性。Miao等[44]采用ASL研究发现,急性期抗NMDAR脑炎患者左侧岛叶、左侧颞上回、左侧海马、左侧苍白球以及双侧壳核和尾状核CBF升高,双侧楔前叶和双侧枕叶CBF降低。同时,与健康对照组比较,存在精神行为异常的抗NMDAR脑炎患者左侧岛叶CBF减低,右侧楔前叶、双侧距状裂周围皮层、双侧舌回的CBF升高,作者认为这些改变可作为抗NMDAR脑炎患者精神行为异常的预测因子。此外,研究发现恢复期抗NMDAR脑炎患者由于血管弹性下降,ASL检查可显示为全脑总CBF、左侧中央前回以及双侧额下回CBF减低[45],提示恢复期患者即使临床症状好转仍存在血流灌注受损。因此,CBF检测可以作为抗NMDAR脑炎患者早期诊断及监测病情发展过程的指标之一。但该序列易受血液流动、磁化传递效应等因素的影响,且对运动造成的误差较为敏感,容易造成结果的偏差[46]。目前已开发出ASL的衍生技术,如供血区ASL可对感兴趣血管进行选择性标记,3D-ASL可得到具有更高空间分辨率的影像,这些技术的应用可从更细微、更直观的角度探测抗NMDAR脑炎血流灌注的改变。

3.4 功能磁共振成像

       功能磁共振成像(functional magnetic resonance imaging, fMRI)主要分为任务态和静息态fMRI,可为大脑功能和心理活动提供生态学上的有效视角,但由于无法客观监控受试者的行为任务表现,不符合研究内容的心理活动可能会导致结果的偏差。

       目前,将任务态fMRI应用于抗NMDAR脑炎的研究较少。一项收集了抗NMDAR脑炎患者完成情景记忆任务时的数据的研究发现,较健康对照组,在神经水平上,患者在记忆编码过程中表现出双侧海马/海马旁回、右侧颞上回和右侧丘脑更高的脑激活,而在行为水平上,患者的记忆功能表现较差。在记忆编码过程中,左侧海马/海马旁回的大脑激活程度越高,患者的记忆能力就越差[47]。这些观察增强了我们对人脑中NMDAR功能障碍的理解。任务态fMRI能直接在受试者接受MRI扫描时评估其认知心理水平,但该方法更依赖于受试者的配合,实施难度更大,因此目前主要应用静息态fMRI方法研究抗NMDAR脑炎。

       静息态fMRI可通过特定指标反映局部神经元自发活动(neuronal spontaneous activity, NSA)和脑功能活动(brain functional activity, BFA)的强度[48],功能连接(functional connection, FC)和局部一致性(regional homogeneity, ReHo)分析是常见的研究脑功能改变的方法。FC可检测出不同空间位置脑区瞬间神经活动的相关性[49],ReHo可反映局部脑区NSA在同一时间序列强度改变的相似程度[50]。Cai等[51]通过FC分析发现,抗NMDAR脑炎患者的双侧扣带回后部、左侧楔前叶、双侧小脑的NSA和BFA减低,且这些改变与认知障碍和情绪调节受损相关;他们还发现双侧扣带回后部与初级视皮层的FC升高,并认为这可能是机体通过增强与记忆相关的视觉脑区的活动来代偿改善记忆功能所致。Li等[52]利用fMRI构建了一个功能性网络,通过分析网络参数的拓扑结构,发现岛叶是抗NMDAR脑炎患者功能性脑网络的中枢,其FC受损影响了顶叶的功能,从而干扰信息的维持、传输和反馈,导致患者认知能力下降。Wu等[53]应用ReHo分析结合多变量模式分析发现,抗NMDAR脑炎患者双侧小脑后叶、小脑前叶、顶下小叶、中脑、尾状核及右侧额上回、颞中回、左侧额中回的ReHo值降低,他们还建立了抗NMDAR脑炎患者的全脑ReHo模式空间分布特征,此分类模型的准确率可达76.83%。此外,结合机器学习算法(如隐马尔可夫模型)研究FC在时间上的波动,以此研究大脑动力学的方法是当前的研究热点[54, 55],但该方法目前尚未应用于抗NMDAR脑炎的相关研究中。

3.5 磁共振波谱

       磁共振波谱(magnetic resonance spectroscopy, MRS)分析可在活体内检测生化和代谢物质,可早期检测到脑代谢异常。基于1H的MRS技术在脑科学研究中应用较多,常用于脑损伤、脑瘤等疾病的诊断和分级,但抗NMDAR脑炎的相关研究中应用较少,多以个案形式报道[56, 57]。既往报道的抗NMDAR脑炎患者的MRS信号特征相似,其异常信号区较对侧正常脑组织比较,均表现为N-乙酰天冬氨酸(N-acetyl aspartate, NAA)峰降低,胆碱(choline, Cho)峰升高,导致Cho/NAA比例倒置。NAA峰的降低提示神经元功能活动减低,Cho峰升高提示细胞破坏或细胞密度增高[58],但此类特征也可见于炎症、感染和肿瘤性疾病,特异性较低。目前MRS对抗NMDAR脑炎的诊断价值有待进一步评估,未来还需更大规模的临床试验以提高对该病的认识。但由于需要预先设置感兴趣区,MRS难以检测全脑广泛的代谢改变,可结合其他适用于全脑的高级MRI,以发现脑内的微小改变。

3.6 影像组学和深度学习

       影像组学和深度学习是目前的前沿热点,可挖掘病灶和全脑的深层特征,但模型的泛化能力很大程度依赖大样本的数据,而抗NMDAR脑炎属于罕见病,收集相对困难。多中心研究可在一定程度上解决该问题,然而目前应用此类方法的抗NMDAR脑炎相关研究仍极少。Xiang等[59]建立了一个结合临床变量、深度学习和影像组学特征的融合模型,以预测成人抗NMDAR脑炎患者的早期功能结果。他们开发了用单个或组合的4个临床 MRI 序列(T1WI、T2WI、T2 FLAIR序列和DWI序列)训练的5个深度学习和放射组学模型,以及一个用临床变量训练的临床模型,以预测抗 NMDAR 脑炎的预后。结果显示融合模型的预测性能显著优于单独的深度学习、影像组学和临床模型。与所有单序列模型相比,深度学习和影像组学的多序列模型具有更高的受试者操作特征曲线下面积值和准确度。

       综上所述,高级MRI进一步发现和解释了部分抗NMDAR脑炎患者常规MRI表现正常而临床症状严重或预后较差的原因。这些技术各有优缺点,合理联合应用各项技术是加深对该病影像学表现及病理和病理生理学改变的认识的有效补充,如Wang等[60]应用形态学分析方法结合DTI和fMRI构建了抗NMDAR脑炎的多模态网络中发现,抗NMDAR脑炎患者功能网络仅有细微变化,而形态网络和结构网络改变较为显著,为抗NMDAR脑炎提供了特征性多模态网络功能障碍的全面视图。

4 总结和展望

       抗NMDAR脑炎是一种发病率逐年上升的自身免疫性疾病,可伴发于肿瘤(以卵巢畸胎瘤多见)或继发于感染性病变(以单纯疱疹病毒性脑炎多见),临床表现复杂多样,确诊依赖于在患者脑脊液和(或)血清中检出相应自身抗体。近半数患者首次常规MRI有异常信号表现,但缺乏特异性。高级 MRI技术可从多角度揭示抗NMDAR脑炎的病理和病理生理学改变,有助于提高对该病的认识。然而,目前对抗NMDAR脑炎研究的样本量均不大,大部分研究也未对不同病程、不同用药方式进行分组,未来应着眼于在大样本的基础上,采用多模态多参数MRI技术进行深入研究。

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