Evaluation of Cognitive Impairment in Patients with Minimal Hepatic Encephalopathy Based on Degree Centrality of Resting-state Blood Oxygenation Level-dependent Functional Magnetic Resonance Imaging

doi:10.12114/j.issn.1007-9572.2022.0828

Chinese General Practice ›› 2023, Vol. 26 ›› Issue (24): 3033-3041.DOI: 10.12114/j.issn.1007-9572.2022.0828

Special Issue: 消化系统疾病最新文章合辑；脑健康最新研究合辑

• Original Research • Previous Articles Next Articles

Evaluation of Cognitive Impairment in Patients with Minimal Hepatic Encephalopathy Based on Degree Centrality of Resting-state Blood Oxygenation Level-dependent Functional Magnetic Resonance Imaging

1. College of Clinical Medicine, Ningxia Medical University, Yinchuan 750004, China
2. Department of Radiology, General Hospital of Ningxia Medical University, Yinchuan 750004, China
3. Department of Infectious Diseases, General Hospital of Ningxia Medical University, Yinchuan 750004, China

Received:2022-09-05 Revised:2023-01-14 Published:2023-08-20 Online:2022-12-20
Contact: WANG Xiaodong

基于静息态血氧水平依赖功能磁共振成像技术的度中心度评价轻型肝性脑病患者认知功能损害的研究

1．750004　宁夏回族自治区银川市，宁夏医科大学临床医学院
2．750004　宁夏回族自治区银川市，宁夏医科大学总医院放射科
3．750004　宁夏回族自治区银川市，宁夏医科大学总医院感染疾病科

通讯作者: 王晓东
作者简介:
作者贡献：杨旭宏负责研究实施、结果分析与解释、文章构思、论文撰写及修订；王明磊、刘文潇、马万龙、丁向春负责数据收集、整理及预处理；赵建国、黄雪莹、王敏行负责统计学处理、研究的实施与可行性分析；王晓东负责论文修订、质量控制及审校，对文章整体负责、监督管理。
基金资助:
宁夏回族自治区自然科学基金资助项目(2022AAC03487); 宁夏回族自治区科技重点研究计划(2019BEG03037); 宁夏医科大学颅脑疾病重点实验室神经科学优势学科群(LNKF202109)

Abstract

Abstract:

Background

Minimal hepatic encephalopathy has atypical clinical symptoms but mild neuropsychiatric deficits, which are easily neglected by patients and their family members as a specific type of hepatic encephalopathy. The degree centrality (DC) analysis method based on resting-state blood oxygenation level-dependent functional magnetic resonance imaging (BOLD-fMRI) is a data analysis method derived from graph-theoretic approach reflecting whole-brain network connectivity, which can provide a more complete, faster and better representation of brain function.

Objective

To explore the effects of abnormal changes in the brain functional network connectivity properties and functional brain regions on cognitive function in patients with minimal hepatic encephalopathy and their neuroimaging mechanisms.

Methods

A total of 65 patients with hepatitis B cirrhosis hospitalized in the department of infectious diseases in General Hospital of Ningxia Medical University from October 2020 to February 2022 and 40 healthy volunteers recruited during the same period were selected as the study subjects. Gender, age, education level, number connection test A (NCT-A) score, digit symbol test (DST) score and Montreal cognitive assessment (MoCA) score of the study subjects were collected. Finally, patients with hepatitis B cirrhosis were divided into cirrhosis group (n=30) and MHE group (n=28) according to NCT-A and DST scores, and the recruited healthy volunteers were considered as the healthy control group (n=34) . The DC values of brain regions in each group were calculate, the differences in DC values of brain image between MHE group and cirrhosis group, cirrhosis group and healthy control group, MHE group and healthy control group were compared, respectively. The correlations between the DC values of brain regions with the scores of NCT-A, DST and MoCA in MHE patients was analyzed by using person correlation analysis, the distribution of brain regions with DC values correlated with the scores of above scales and the corresponding scatter plots were drawn.

Results

The NCT-A score in the healthy control and cirrhotic group was lower than MHE group, DST score and MoCA score in the healthy control and cirrhotic group were higher than MHE group (P<0.05) . Compared with healthy control group, the MHE group had increased DC values in right middle frontal gyrus, left middle temporal gyrus, right inferior parietal lobule and decreased DC values in left angular gyrus, right middle occipital gyrus, right precentral gyrus (voxel cluster>18, P<0.05) . Compared with healthy control group, cirrhotic group had increased DC values in the bilateral middle temporal gyrus and decreased DC values in the left angular gyrus (voxel cluster>18, P<0.05) ; compared with cirrhotic group, MHE group had decreased values in the right middle temporal gyrus and left precuneus (voxel cluster>18, P<0.05) . The results of correlation analysis showed that in the MHE group, the DST score was correlated with DC values in the left superior temporal gyrus (r=0.639, P<0.001) , and the NCT-A score was negatively correlated with the DC values in the right inferior temporal gyrus (r=-0.722, P<0.001) ; MoCA scale score was positively correlated with DC values in the right inferior frontal gyrus and left inferior frontal gyrus (r=0.437, P=0.020; r=0.549, P=0.002) and negatively correlated with DC values in the left inferior temporal gyrus (r=-0.591, P=0.001) .

Conclusion

The abnormal functional connectivity of several brain regions and the correlation of DC values in some brain regions with NCT-A, DST and MoCA scale scores in MHE patients suggest that DC value may be a potential neuroimaging marker to quantify the severity of cognitive changes in MHE patients.

Key words: Hepatic encephalopathy, Minimal hepatic encephalopathy, Magnetic resonance imaging, Blood oxygenation level dependent functional magnetic resonance imaging, Degree centrality, Cognitive impairment, Cognition disorders

摘要：

背景

轻型肝性脑病（MHE）作为肝性脑病的一个特殊类型，临床症状不典型，且存在轻度神经、精神缺陷，易被患者及家属忽视。基于静息态血氧水平依赖功能磁共振成像（BOLD-fMRI）技术的度中心度（DC）分析方法是从图论方法衍生而来的一种反映全脑网络连接的数据分析方法，其能更完整、更快捷、更好地体现大脑功能。

目的

基于BOLD-fMRI技术的DC分析方法探究MHE患者脑功能网络连接属性的异常改变及功能脑区的异常变化对患者认知功能的影响及其神经影像机制。

方法

选取2020年10月—2022年2月在宁夏医科大学总医院感染疾病科住院的65例乙型肝炎肝硬化患者及同期招募的40例健康志愿者为研究对象，收集研究对象的性别、年龄、教育程度、数字连接实验A（NCT-A）评分、数字符号实验（DST）评分和蒙特利尔认知评估量表（MoCA）评分，根据NCT-A及DST评分最终将乙型肝炎肝硬化患者分为肝硬化组（n=30）和MHE组（n=28），招募的健康志愿者纳入健康对照组（n=34）。计算各组脑区的DC值，比较MHE组与肝硬化组、肝硬化组与健康对照组、MHE组与健康对照组脑图的DC值差异，采用Person相关分析法分析MHE患者脑区DC值与NCT-A、DST和MoCA评分的相关性，并绘制不同脑区DC值与上述量表存在相关性的脑区分布及对应散点图。

结果

健康对照组和肝硬化组的NCT-A评分低于MHE组，DST、MoCA评分高于MHE组（P<0.05）。与健康对照组相比，MHE组右侧额中回、左侧颞中回以及右侧顶下小叶DC值升高，左侧角回、右侧枕中回和右侧中央前回DC值减低（体素簇>18，P<0.05）；与健康对照组相比，肝硬化组双侧颞中回DC值升高，左侧角回DC值降低（体素簇>18，P<0.05）；与肝硬化组相比，MHE组右侧颞中回，左侧楔前叶DC值降低（体素簇>18，P<0.05）。相关性分析结果显示，MHE组DST评分与左侧颞上回的DC值呈正相关（r=0.639，P<0.001），NCT-A评分与右侧颞下回的DC值呈负相关（r=-0.722，P<0.001）；MHE组MoCA评分与右侧额下回和左侧额下回的DC值呈正相关（r=0.437，P=0.020；r=0.549，P=0.002），与左侧颞下回的DC值呈负相关（r=-0.591，P=0.001）。

结论

MHE患者多个脑区功能连接异常且部分脑区DC值与NCT-A、DST以及MoCA量表评分相关，提示DC值可能是量化MHE患者认知功能改变严重程度的潜在神经影像标志物。

关键词: 肝性脑病, 轻型肝性脑病, 磁共振成像, 静息态血氧水平依赖功能磁共振成像, 度中心度, 认知功能损害, 认知障碍

YANG Xuhong,WANG Minglei,LIU Wenxiao, et al. Evaluation of Cognitive Impairment in Patients with Minimal Hepatic Encephalopathy Based on Degree Centrality of Resting-state Blood Oxygenation Level-dependent Functional Magnetic Resonance Imaging[J]. Chinese General Practice, 2023, 26(24): 3033-3041. DOI: 10.12114/j.issn.1007-9572.2022.0828.
杨旭宏,王明磊,刘文潇等. 基于静息态血氧水平依赖功能磁共振成像技术的度中心度评价轻型肝性脑病患者认知功能损害的研究[J]. 中国全科医学, 2023, 26(24): 3033-3041. DOI: 10.12114/j.issn.1007-9572.2022.0828.

Figures/Tables 6

References 34

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扫描序列	3D-T1 BRAVO	BOLD-fMRI
重复时间（ms）	7.7	2 000
回波时间（ms）	3.1	30
翻转角	12°	90°
视野（mm）	240×240	250×250
矩阵	256×256	64×64
层厚（mm）	1.2	3.6
层数	136	35
扫描时间（s）	215	360

扫描序列	3D-T1 BRAVO	BOLD-fMRI
重复时间（ms）	7.7	2 000
回波时间（ms）	3.1	30
翻转角	12°	90°
视野（mm）	240×240	250×250
矩阵	256×256	64×64
层厚（mm）	1.2	3.6
层数	136	35
扫描时间（s）	215	360

组别	例数	性别（男/女）	年龄（±s，岁）	受教育年限（±s，年）	NCT-A评分（±s，s）	DST评分（±s，分）	MoCA评分（±s，分）
健康对照组	34	24/10	44.6±7.1	7.9±1.6	36.3±8.4^b	46.3±9.6^b	26.6±1.8^b
肝硬化组	30	18/12	46.9±9.2	8.1±1.5	38.4±13.4^b	43.2±5.0^b	26.2±1.8^b
MHE组	28	19/9	47.0±9.3	7.8±1.6	70.0±14.0	21.1±5.0	20.3±3.6
F（χ²）值		0.843^a	0.801	0.952	72.473	117.516	59.567
P值		0.656	0.452	0.392	<0.001	<0.001	<0.001

组别	例数	性别（男/女）	年龄（±s，岁）	受教育年限（±s，年）	NCT-A评分（±s，s）	DST评分（±s，分）	MoCA评分（±s，分）
健康对照组	34	24/10	44.6±7.1	7.9±1.6	36.3±8.4^b	46.3±9.6^b	26.6±1.8^b
肝硬化组	30	18/12	46.9±9.2	8.1±1.5	38.4±13.4^b	43.2±5.0^b	26.2±1.8^b
MHE组	28	19/9	47.0±9.3	7.8±1.6	70.0±14.0	21.1±5.0	20.3±3.6
F（χ²）值		0.843^a	0.801	0.952	72.473	117.516	59.567
P值		0.656	0.452	0.392	<0.001	<0.001	<0.001

Evaluation of Cognitive Impairment in Patients with Minimal Hepatic Encephalopathy Based on Degree Centrality of Resting-state Blood Oxygenation Level-dependent Functional Magnetic Resonance Imaging

基于静息态血氧水平依赖功能磁共振成像技术的度中心度评价轻型肝性脑病患者认知功能损害的研究

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相关脑区	位置	体素簇	MNI坐标			t值
相关脑区	位置	体素簇	X	Y	Z	t值
MHE组与健康对照组
额中回（升高）	右	27	33	0	48	3.760
颞中回（升高）	左	37	-39	-57	21	-3.901
顶下小叶（升高）	右	43	51	-36	21	3.530
枕中回（降低）	右	33	26	-92	12	-3.918
角回（降低）	左	27	-40	-52	22	-3.900
中央前回（降低）	右	25	2	-27	57	-3.968
肝硬化组与健康对照组
颞中回（升高）	左	51	-57	-60	-6	3.973
颞中回（升高）	右	121	66	-51	-9	5.117
角回（降低）	左	19	-44	-55	20	-3.331
MHE组与肝硬化组
楔前叶（降低）	左	22	-13	-71	26	-3.464
颞中回（降低）	右	25	59	-56	-3	-3.870

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