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综述
脊髓损伤患者认知损害及其神经影像学研究进展
汪晶 李伦兰 廖晨霞 张凡 高馨

Cite this article as: Wang J, Li LL, Liao CX, et al. Research progress of cognitive impairment and neuroimaging in patients with spinal cord injury[J]. Chin J Magn Reson Imaging, 2022, 13(3): 134-137.本文引用格式:汪晶, 李伦兰, 廖晨霞, 等. 脊髓损伤患者认知损害及其神经影像学研究进展[J]. 磁共振成像, 2022, 13(3): 134-137. DOI:10.12015/issn.1674-8034.2022.03.033.


[摘要] 脊髓损伤后认知损害的发生率较高,但因不易察觉而可能被忽略,且脊髓损伤后认知损害与多种因素相关,大脑结构功能的改变可能实际参与了认知损害过程,但具体机制尚不清楚。近年来学者采用神经影像学方法对脊髓损伤后脑结构功能改变进行研究,以期阐明脊髓损伤后认知损害机制。本文对脊髓损伤患者认知损害发病率及临床特征、评估方法、影响因素及神经影像学改变进行综述,旨在为脊髓损伤患者认知损害的预防及干预提供参考。
[Abstract] The incidence of cognitive impairment after spinal cord injury is high, but it may be ignored because it is not easy to detect. Moreover, the cognitive impairment after spinal cord injury is related to a variety of factors, among which the change of brain structure and function may actually be involved in the process of cognitive impairment, but the specific mechanism remains unclear. In recent years, scholars have used neuroimaging methods to study the changes of brain structure and function after spinal cord injury, in order to clarify the mechanism of cognitive impairment after spinal cord injury.This article reviews the incidence, clinical features,assessment methods,main influencing factors and neuroimaging changes of cognitive impairment in patients with spinal cord injury, aiming to provide reference for the prevention and intervention of cognitive impairment in patients with spinal cord injury.
[关键词] 脊髓损伤;认知损害;神经影像学;功能磁共振成像;研究进展
[Keywords] spinal cord injury;cognitive impairment;neuroimaging;functional magnetic resonance imaging;research progress

汪晶    李伦兰 *   廖晨霞    张凡    高馨   

安徽医科大学第一附属医院脊柱外科,合肥 230022

李伦兰,E-mail:lilunlan@aliyun.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: 安徽省2019年重点研究与开发计划项目 201904a07020048 安徽省高校自然科学研究项目 KJ2020ZD18
收稿日期:2021-08-21
接受日期:2022-02-07
中图分类号:R445.2  R744  R749.2 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2022.03.033
本文引用格式:汪晶, 李伦兰, 廖晨霞, 等. 脊髓损伤患者认知损害及其神经影像学研究进展[J]. 磁共振成像, 2022, 13(3): 134-137. DOI:10.12015/issn.1674-8034.2022.03.033

       脊髓损伤(spinal cord injury,SCI)是指各种原因引起的脊髓结构和功能损害,并造成损伤水平以下运动、感觉、自主神经功能障碍的一类严重损伤[1]。随着全球经济的发展,SCI发病率逐年上升[2],SCI患者损伤后需要高昂的医疗支出,估计终生医疗费用为100万~300万美元,给家庭和社会带来巨大的经济负担,已成为世界范围内的主要公共卫生问题[3]。SCI是使患者生理心理遭受严重创伤的应激性事件,不仅造成运动、感觉功能障碍,同时造成认知功能损害[4, 5]。SCI患者损伤后需要适应新的生活方式、获得自我照顾方法和重新融入社区的能力,这些可能会受到认知损害的干扰,从而影响患者达到最佳的康复结果[6]。近年来,国内外学者通过动物实验模型及神经影像学方法对SCI患者认知损害可能机制展开研究,发现SCI患者认知损害与脑部结构功能改变有关[7, 8]。本文对SCI患者认知损害发病率及临床特征、评估方法、影响因素及神经影像学改变进行综述,旨在为SCI患者认知功能损害的预防及干预提供参考。

1 SCI与认知损害

1.1 SCI患者认知损害发生率及临床特征

       国外学者针对SCI患者认知损害的研究最早起源于20世纪60年代[9],Davidoff及相关研究者通过综合神经心理学成套测验发现40%~50%的SCI患者有不同程度和表现的认知损害[10, 11, 12, 13]。后来学者使用单项测试方法,对SCI患者认知损害进行研究,Borgaro等[14]发现35.3%的SCI患者存在时间定向障碍,Holtslag等[15]研究发现SCI患者认知损害发生率高达75%。Cohen等[16]对SCI患者和156名健康对照者进行配对研究,发现SCI患者在处理速度、执行功能和情景记忆方面的表现比对照组差,且25%的患者存在执行功能方面的损害。Craig等[17]采用同样的研究方法发现28.6%的SCI患者存在认知障碍,而16.6%的患者有更严重的认知损害。此外,SCI患者发生认知损害的风险是非SCI人群的12.9倍。Sachdeva等[18]通过对近年来针对SCI患者认知损害的70项研究进行系统回顾,发现其中38项研究均报告了SCI患者存在一个或多个领域的认知损害,SCI患者认知损害的发生率高达64%。国内学者[19, 20]针对SCI认知损害的研究起步较晚,且多以制造出SCI大鼠模型,通过Morris水迷宫等测试证实SCI可造成认知损害,针对SCI患者人群认知损害的研究尚未报道。关于SCI患者认知损害的主要表现,各项研究结果较为相似,可归纳为记忆力减退、集中注意力困难、执行能力减退及在抽象推理、学习新知识等方面遭遇困难[10, 11, 12, 13]。综上,SCI患者认知功能损害较为普遍,但因为研究设计、样本量及评估方法存在异质性,SCI患者认知损害发生率尚未有确切的结论。

1.2 SCI患者认知功能评估方法

       自研究提出SCI可造成认知功能损害以来,许多认知测试方法或工具被用于量化SCI患者的认知功能,评估的认知领域包括记忆、执行功能、语言、视觉空间能力、信息处理、注意力和学习等。在这些测试方法中,功能独立性测量(functional independence measure,FIM)认知子量表、美国国立卫生研究院的认知工具箱(National Institutes of Health Toolbox Cognition Battery,NIHTB-CB)和神经精神科认知评估工具(Neuropsychiatry Unit Cognitive Assessment Tool,NUCOG)是最早被熟知用于SCI患者认知损害的基本筛查工具[16, 17,21]。但近期研究认为FIM认知子量表并不适用于SCI患者的认知功能评估,因为其评分存在天花板效应[21]。NIHTB-CB可反映研究对象过去的学习经验以及学习新知识和信息处理的能力,任何年龄段均适用,但用于上肢有损伤的SCI患者可能存在局限性[22]。NUCOG用于评估认知功能的5个领域,包括记忆、注意、执行、视觉结构和语言,需要评估对象具备运动功能,这对于存在运动功能障碍的SCI患者适用性较低。因此,后期学者使用全面的神经心理学评估工具,如Stroop测试、连线测试(Trail Making Test,TMT A&B)、数字广度测试(Digit Span Task,DST)、雷伊听觉语言学习测试(Rey Auditory-Verbal Learning Test,RAVLT)等评估SCI患者的认知功能,此类评估工具可用于特定认知领域的功能筛查[23, 24, 25]。经研究证实其在SCI患者认知功能评估中均具有较好的重测信度[26]。此外,电生理技术也可应用于认知功能评估中,早期的一项研究发现,特异性记忆力减退与神经障碍患者的P300振幅下降有关[27]。然而,SCI患者特异性认知障碍和P300变化之间的潜在联系仍有待于研究,以期为存在此类认知障碍的患者提出更好的康复方案。

2 SCI患者认知损害影响因素

2.1 创伤性脑损伤

       早期对SCI后认知损害影响因素的研究多集中于创伤性脑损伤(traumatic brain injury,TBI),认为其是SCI后认知损害的主要原因[28, 29, 30]。研究表明[30] 16%~59%的SCI患者同时伴有TBI,这可能是引起SCI后认知损害的直接原因。Bradbury等[29]通过比较单纯SCI患者和SCI伴TBI患者的认知功能,结果显示SCI伴TBI患者比单纯SCI患者表现出更严重的认知损害。但Hess等[31]的研究指出TBI对SCI后认知功能的影响与TBI的严重程度有关,中重度TBI与SCI认知损害有关,而轻度TBI对SCI认知功能几乎无影响。在Mollayeva等[32]最新的研究中,通过控制其他危险因素,发现SCI伴TBI会增加痴呆的风险。虽然上述研究结果存在差异,但显然的是,TBI会加重SCI后的认知功能损害。

2.2 其他因素

       除上述因素外,SCI后认知损害相关因素还有很多。首先,自主神经系统(autonomic nervous system,ANS)功能障碍在SCI患者中也较为普遍,可能是引起SCI后认知损害的另一重要原因。自主神经系统功能障碍的特征表现为血压骤升或骤降,难以维持平衡[25,33]。Sachdeva等[33]研究表明,系统性血压不稳定波动与广泛的认知损害有关,可能是因为高低血压发作时,无法维持和调整脑血流量以满足大脑的代谢需求。其次,SCI患者受伤前即存在的学习障碍、或药物滥用、较低的文化程度以及性别、年龄均会影响认知功能[17, 18]。最后,损伤后继发性的并发症也会影响患者认知功能,如阻塞性睡眠呼吸暂停(obstructive sleep apnea,OSA)、焦虑抑郁、慢性疼痛、药物副作用、疲劳等[17, 18,34]。研究表明[34]近50%的高位损伤SCI患者存在阻塞性睡眠呼吸暂停,其严重程度与认知损害呈正相关。多项研究表明焦虑、抑郁、疼痛、疲乏等是SCI患者认知损害的预测因素,尤其是在患者出院六个月以后融入社会,其认知功能损害与焦虑、抑郁水平显著相关[17, 18]。综上,SCI患者认知损害受多种因素的影响,为了能够及时对SCI后认知损害进行诊断和干预,探索SCI后认知损害的可能机制是亟待解决的问题。

3 SCI患者认知损害的神经影像学特征

       作为中枢神经系统范围内的一类损伤,SCI引起的改变不仅仅局限于损伤部位,同时引起与脊髓结构与功能紧密相连的大脑皮层发生重组,SCI后认知损害可能与大脑皮层的重组有关[35, 36, 37]。随着影像医学技术的发展,多模态磁共振技术可以观察并量化脑部结构及功能的改变,作为一种神经影像学标志物为临床疾病的诊断提供帮助,已广泛应用于阿尔茨海默病、轻度认知功能障碍及抑郁症等神经精神疾病中[38, 39]。目前应用于SCI患者脑结构功能改变的研究方法包括结构磁共振成像(stracture MRI,sMRI)、扩散张量成像(diffusion tensor imaging,DTI)、静息态功能磁共振成像(resting-state functional MRI,rs-fMRI)等。其中脑结构成像及DTI分析方法为基于体素形态学(voxel-based morphometry,VBM)和基于束的空间统计分析(tract-based spatial statistics,TBSS)以定量计算脑灰质、白质体积及结构变化;rs-fMRI通过获取脑血流灌注或神经元活动情况以量化大脑功能[40, 41, 42]

3.1 脑结构改变

       早期的多项动物实验及人类研究证实SCI后与其直接相关区域的脑结构发生萎缩,如双侧初级运动皮层及初级感觉皮层,表现为灰质体积的减少[35, 36, 37]。但后来的研究发现,除了感觉运动皮质的退行性变化外,SCI还可导致非感觉运动皮质的萎缩,如前扣带皮质、岛叶皮质、额中回、颞中回等重要脑区,这些脑区的功能与人类的感觉、运动、认知、情绪等密切相关[43, 44, 45, 46, 47]。Wrigley等[43]应用VBM分析,发现与健康对照组相比,SCI患者双侧初级运动皮层灰质体积显著降低(P<0.05),同时,内侧前额叶和邻近的前扣带也显著降低(P<0.05),这些差异性区域覆盖在受试者的T1加权解剖扫描上。Hou等[44]研究SCI患者损伤早期的脑结构改变,发现SCI患者存在更多脑区的结构显著萎缩,包括双侧初级运动皮层及初级感觉皮层,以及辅助运动区、丘脑。该学者进一步分析了萎缩脑区对临床指标的影响,显示双侧初级运动皮层中灰质体积与运动评分显著相关(左r2=0.49,P<0.001;右r2=0.38,P=0.003),可见,SCI后脑结构萎缩对患者的功能恢复产生了影响,这点在临床可能被忽略。Chen等[45]同样采用对照研究探究SCI患者脑结构的改变,发现SCI患者脑部显著网络存在灰质萎缩,主要表现在背侧前扣带、双侧前岛、双侧眶额和右侧颞上回。双侧前岛和背侧前扣带均为显著网络的核心枢纽,负责识别相关显著刺激,并将其传达给更高的认知区域以指导做出行为反应[48, 49],这些显著网络的结构萎缩可能引起更高级的认知损害。近期的一项研究[46]结果发现与健康对照组相比,SCI患者灰质萎缩集中在额叶相关区域,如额中回、左侧额上回以及左侧额内侧回。额叶功能为参与执行功能和认知过程,因此推测,额叶结构改变可能与SCI后执行功能方面认知损害密切相关[50]。SCI后不仅引起灰质体积的缩小,也引起白质微结构的改变。Hou等[44]研究中,SCI患者的感觉运动系统灰质萎缩的同时,双侧脑梗水平的皮质脊髓束白质也发生萎缩。Guo等[47]通过DTI技术研究患者和健康对照者的脑白质微结构差异,发现SCI患者胼胝体、后丘脑辐射,右扣带、额枕上束等脑区白质结构完整性被破坏。胼胝体的完整性破坏会导致记忆、执行功能和处理速度等领域的认知功能障碍[51]。因此,SCI患者普遍存在的记忆力下降,可能与扣带回白质损伤有关。一项关于SCI患者灰质白质体积改变研究的荟萃分析得出了相似的结论,即SCI后脑结构发生了显著萎缩[52],且显著网络区域的结构萎缩可能是SCI患者神经性疼痛和认知、情绪障碍等症状的原因[53, 54, 55]。以上研究说明了SCI后脑结构发生萎缩,这可能是SCI患者认知损害的结构基础。

3.2 脑功能改变

       虽然关于SCI后神经影像学的研究多集中于脑结构的改变,但近年来涉及SCI后脑功能改变的研究也逐渐增多[56, 57, 58, 59, 60, 61]。Zhu等[56]采用静息态磁共振对急性SCI患者和健康对照者进行扫描,依据局部一致性(regional homogeneity,ReHo)评价自发神经活动改变,结果显示与健康对照组相比,SCI患者的双侧初级运动感觉皮质、双侧辅助运动区神经活动降低,且与认知功能密切相关的脑区如额回、双侧尾状核以及背侧前扣带回的神经活动也显著降低。Hou等[57, 58]研究采用低频振荡振幅(amplitude of low-frequency fluctuations,ALFF)探究SCI患者异常神经活动,并分析异常神经活动与损伤6个月后运动功能评分之间的相关性,结果发现SCI患者双侧初级运动感觉皮质神经活动降低,而双侧小脑和右侧眶额皮质神经活动增加,且SCI患者小脑神经活动增加与损伤6个月后的运动评分呈负相关(r2=0.56,P<0.001)。Hawasli等[59]通过选取不同的种子点分析SCI患者脑区功能连接(function connectivity,FC),结果发现SCI患者脑区各重要网络之间的功能连接降低(如默认网络、显著网络、控制网络等),且各脑区功能连接随时间发生负向变化。以上研究揭示临床应尽早关注SCI患者脑部功能改变并及时进行干预,这可能是改善患者预后的重要举措。赵莹[60]研究中,对脊髓型颈椎病患者及健康对照者双侧海马种子区与全脑其他脑区作基于体素的时间序列相关性分析,发现静息态下脊髓型颈椎病患者在记忆、视觉和语言功能有重要作用的脑区与双侧海马之间功能连接存在异常(P<0.05),由此可见,脊髓部位的损伤不仅表现在局部或损伤平面以下,对上行脑区也产生了显著影响。Sachdeva等[61]通过大鼠实验研究发现SCI组大鼠海马区血流量较正常组大鼠减少了32%,且SCI组大鼠伴有短期记忆障碍。因此,这些对认知功能起着重要作用的脑区与双侧海马之间功能连接异常以及血流量异常等脑功能改变可能是引起SCI患者认知损害的基础。

       综上所述,SCI后脑结构功能发生显著性改变,其中重要脑区的改变可能参与了SCI后认知损害。因为采用的研究方法、研究指标、研究对象损伤时间不同,结果存在一定的差异,且SCI后是否引起某一特定脑区结构功能的改变,以及对认知功能的影响机制尚不清楚,未来还有待探索。同时,目前对SCI后脑结构和功能改变的研究多为独立,然而一定的功能改变必定以结构改变为基础,结构改变往往又带来相应的功能变化,因此,未来可同时对SCI患者脑结构与功能改变与认知损害之间的相关性展开进一步的研究。

4 小结与展望

       SCI发生后,不仅造成患者肢体功能障碍,同时存在一定程度的认知损害,影响患者预后。虽然,目前对于SCI患者的研究已扩大到认知功能,但由于SCI后认知损害受多种复杂因素影响,且我们对SCI后认知损害的研究还处于初步阶段,同时SCI后导致的脑结构功能改变及其与认知损害之间的关系尚不清楚。因此,未来对SCI患者的治疗与康复策略不仅仅侧重于提高肢体功能,还应关注提高认知功能,同时提示可及时通过神经影像学方法评估SCI后脑结构功能的改变,探究其导致认知损害的相关机制,寻找神经影像学标志物,以期为SCI患者治疗及预后提供依据。

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