Prediction study of white matter microstructural changes on long-term cognitive impairment in patients with acute ischemic stroke

doi:10.3877/cma.j.issn.2095-123X.2024.04.001

Abstract

Abstract:

Objective

To analyze the evolution of white matter microstructural integrity in acute ischemic stroke (AIS) patients with impaired cognitive functions using diffusion tensor imaging (DTI) and post-processing method based on tract based spatial statistics (TBSS), and to explore imaging biomarkers for early prediction of post-stroke cognitive impairment (PSCI).

Methods

A prospective study was conducted on 55 patients with cognitive impairment within 3 d after AIS who were hospitalized or followed up in the Neurology Department of Wusong Branch, Zhongshan Hospital Affiliated to Fudan University from August 2021 to April 2023.DTI scans and cognitive assessments were performed on all patients before and 6 months after treatment.According to the cognitive scores after 6 months, patients were divided into PSCI group and post-stroke non-cognitive impairment (N-PSCI)group.By TBSS,horizontally analyzed the differences in fractional anisotropy (FA) and mean diffusivity (MD) between two groups, and vertically analyzed the changes in FA and MD values before and 6 months after treatment within the group.

Results

Among the 55 patients, 4 patients lost contact, 3 patients refused further participation,and 1 patient died,47 patients were enrolled,including 22 in the PSCI group and 25 in the N-PSCI group.Compared with baseline, cognitive performance improved in 33 patients and remained unchanged in 14 patients after 6 months of treatment.Horizontal analysis between groups showed that the FA value of right superior longitudinal fasciculus (SLF) in the PSCI group was lower than that in the N-PSCI group before treatment, and the difference was statistically significant (P＜0.05).Longitudinal analysis showed that the dispersion of multiple white matter tracts (SLF, anterior thalamic radiation, corticospinal tract, etc.)recorded after 6 months of treatment worsened than those recorded before treatment in both groups with statistically significant (P＜0.05).

Conclusion

Patients with baseline impaired cognitive functions still have white matter microstructural damages at 6 months, even if their cognitive function has improved or returned to normal, which may have a negative impact on long-term cognition.The change of FA value of the right SLF fiber bundle has a certain predictive effect on the occurrence of PSCI.

Key words: Acute ischemic stroke, Cognitive impairment, Diffusion tensor imaging, Tract based spatial statistics, Superior longitudinal fasciculus

Li Ji, Yunnan Su, Bin Wang, Tao Shen, Tuanjie Liu, Lei Mao, Yuping Xu, Ting Zhang, Bo Wang. Prediction study of white matter microstructural changes on long-term cognitive impairment in patients with acute ischemic stroke[J]. Chinese Journal of Brain Diseases and Rehabilitation(Electronic Edition), 2024, 14(04): 193-200.

/ / Recommend

Add to citation manager EndNote|Ris|BibTeX

URL: https://zhnkjbykfzz.cma-cmc.com.cn/EN/10.3877/cma.j.issn.2095-123X.2024.04.001

https://zhnkjbykfzz.cma-cmc.com.cn/EN/Y2024/V14/I04/193

Figures/Tables 7

References 24

[1]	Liao XL, Zuo LJ, Zhang N, et al.The occurrence and longitudinal changes of cognitive impairment after acute ischemic stroke[J].Neuropsychiatr Dis Treat, 2020, 16: 807-814.DOI: 10.2147/ndt.S234544.
[2]	Molad J, Hallevi H, Korczyn AD, et al.Vascular and neurodegenerative markers for the prediction of post - stroke cognitive impairment: results from the TABASCO study[J].J Alzheimers Dis,2019,70(3):889-898.DOI:10.3233/jad-190339.
[3]	Sagnier S, Catheline G, Dilharreguy B, et al.Normal-appearing white matter deteriorates over the year after an ischemic stroke and is associated with global cognition[J].Transl Stroke Res,2022,13(5):716-724.DOI:10.1007/s12975-022-00988-8.
[4]	Sagnier S, Catheline G, Dilharreguy B, et al.Normal-appearing white matter integrity is a predictor of outcome after ischemic stroke[J].Stroke, 2020, 51(2): 449-456.DOI: 10.1161/strokeaha.119.026886.
[5]	Zamboni G, Griffanti L, Jenkinson M, et al.White matter imaging correlates of early cognitive impairment detected by the Montreal cognitive assessment after transient ischemic attack and minor stroke[J].Stroke,2017,48(6):1539-1547.DOI:10.1161/strokeaha.116.016044.
[6]	惠子欣,张军.弥散张量成像对重复经颅磁刺激治疗缺血性脑卒中偏瘫患者的疗效评估[J].中华脑科疾病与康复杂志(电子版), 2022, 12(4): 204-209.DOI: 10.3877/cma.j.issn.2095-123X.2022.04.003.Hui ZX, Zhang J.Evaluate the therapeutic efficacy by diffusion tensor imaging for ischemic stroke hemiplegia patients treated with repetitive transcranial magnetic stimulation[J].Chin J Brain Dis Rehabil (Electronic Edition), 2022, 12(4): 204-209.DOI: 10.3877/cma.j.issn.2095-123X.2022.04.003.
[7]	Zhang Q, Yan X, Du J, et al.Diffusion tensor imaging as a tool to evaluate the cognitive function of patients with vascular dementia:a meta-analysis[J].Neurologist, 2023, 28(3): 143-149.DOI: 10.1097/nrl.0000000000000461.
[8]	魏微,何江弘,黄勇华,等.脑成像技术在意识障碍患者脑功能评估中的应用[J].中华神经创伤外科电子杂志,2022,8(2):117-120.DOI:10.3877/cma.j.issn.2095-9141.2022.02.011.Wei W, He JH, Huang YH, et al.Application of neuroimaging technologies in assessment of brain function for patients with disorders of consciousness[J].Chin J Neurotrauma Surg(Electronic Edition),2022,8(2):117-120.DOI:10.3877/cma.j.issn.2095-9141.2022.02.011.
[9]	Hu X,Zhang L,Bu X,et al.White matter disruption in obsessivecompulsive disorder revealed by meta-analysis of tract-based spatial statistics[J].Depress Anxiety, 2020, 37(7): 620-631.DOI:10.1002/da.23008.
[10]	He C, Gong M, Li G, et al.Evaluation of white matter microstructural alterations in patients with post-stroke cognitive impairment at the sub-acute stage[J].Neuropsychiatr Dis Treat,2022,18:563-573.DOI:10.2147/ndt.S343906.
[11]	Mastropietro A, Rizzo G, Fontana L, et al.Microstructural characterization of corticospinal tract in subacute and chronic stroke patients with distal lesions by means of advanced diffusion MRI[J].Neuroradiology, 2019, 61(9): 1033-1045.DOI: 10.1007/s00234-019-02249-2.
[12]	贺春雪,娄明武,韩冰,等.亚急性期缺血性卒中后非痴呆认知障碍患者的弥散张量成像研究[J].中国康复医学杂志, 2022,37(1):68-74.DOI:10.3969/j.issn.1001-1242.2022.01.013.He CX, Lou MW, Han B, et al.Diffusion tensor imaging of nondementia cognitive impairment following subacute ischemic stroke[J].Chin J Rehabil Med, 2022, 37(1): 68-74.DOI: 10.3969/j.issn.1001-1242.2022.01.013.
[13]	Hagberg G, Fure B, Thommessen B, et al.Predictors for favorable cognitive outcome post-stroke: a-seven-year follow-up study[J].Dement Geriatr Cogn Disord,2019,48(1-2):45-55.DOI:10.1159/000501850.
[14]	Bujang MA.A step-by-step process on sample size determination for medical research[J].Malays J Med Sci, 2021, 28(2): 15-27.DOI:10.21315/mjms2021.28.2.2.
[15]	中华医学会老年医学分会老年神经病学组,老年人认知障碍诊治专家共识撰写组.中国老年人认知障碍诊治流程专家建议[J].中华老年医学杂志, 2014, 33(8): 817-825.DOI: 10.3760/cma.j.issn.0254-9026.2014.08.001.Geriatric Neurology Group, Geriatric Society of Chinese Medical Association, Expert Consensus Writing Group on Diagnosis and Treatment of Cognitive Impairment in The Elderly.Chinese experts'recommendation on the diagnosis and treatment of cognitive impairment in the elderly[J].Chin J Geriatr, 2014, 33(8): 817-825.DOI:10.3760/cma.j.issn.0254-9026.2014.08.001.
[16]	Park HY, Park CR, Suh CH, et al.Diagnostic performance of the medial temporal lobe atrophy scale in patients with Alzheimer's disease: a systematic review and meta-analysis[J].Eur Radiol,2021,31(12):9060-9072.DOI:10.1007/s00330-021-08227-8.
[17]	Weaver NA, Kuijf HJ, Aben HP, et al.Strategic infarct locations for post - stroke cognitive impairment: a pooled analysis of individual patient data from 12 acute ischaemic stroke cohorts[J].Lancet Neurol, 2021, 20(6): 448-459.DOI: 10.1016/s1474-4422(21)00060-0.
[18]	中国卒中学会卒中后认知障碍研究圆桌会议专家组.中国卒中后认知障碍防治研究专家共识[J].中国卒中杂志,2020,15(2):158-166.DOI:10.3969/j.issn.1673-5765.2020.02.010.Chinese Stroke Association Poststroke Cognitive Impairment Research Roundtable Experts Group.Expert consensus on prevention and treatment of post-stroke cognitive impairment in China[J].Chin J Stroke, 2020, 15(2): 158-166.DOI: 10.3969/j.issn.1673-5765.2020.02.010.
[19]	Oh EY, Jung MS.Effects of a cognitive training program on cognitive function and activities of daily living in patients with acute ischemic stroke[J].J Korean Acad Nurs, 2017, 47(1): 1-13.DOI:10.4040/jkan.2017.47.1.1.
[20]	Cha J, Kim ST, Jung WB, et al.Altered white matter integrity and functional connectivity of hyperacute-stage cerebral ischemia in a rat model[J].Magn Reson Imaging, 2016, 34(8): 1189-1198.DOI:10.1016/j.mri.2016.04.004.
[21]	Wassenaar TM, Yaffe K, van der Werf YD, et al.Associations between modifiable risk factors and white matter of the aging brain: Insights from diffusion tensor imaging studies[J].Neurobiol Aging, 2019, 80: 56-70.DOI: 10.1016/j.neurobiolaging.2019.04.006.
[22]	Koshiyama D, Fukunaga M, Okada N, et al.Association between the superior longitudinal fasciculus and perceptual organization and working memory: a diffusion tensor imaging study[J].Neurosci Lett, 2020, 738: 135349.DOI: 10.1016/j.neulet.2020.135349.
[23]	Wu B, Guo S, Jia X, et al.White matter microstructural alterations over the year after acute ischemic stroke in patients with baseline impaired cognitive functions[J].Neural Plast, 2023,2023:6762225.DOI:10.1155/2023/6762225.
[24]	Qin L,Guo Z,McClure MA,et al.White matter changes from mild cognitive impairment to Alzheimer' s disease: a meta-analysis[J].Acta Neurol Belg,2021,121(6):1435-1447.DOI:10.1007/s13760-020-01322-5.

项目	PSCI组（n=22）	N-PSCI组（n=25）	t/χ²/U值	P值
年龄（岁，Mean±SD）	63.73±3.69	62.56±4.70	0.937	0.354
性别（男/女）	13/9	11/14	1.066	0.302
受教育年限（年，Mean±SD）	9.55±0.86	9.96±1.14	-1.396	0.169
高血压病[例（%）]	16（72.73）	15（60.00）	0.844	0.358
糖尿病[例（%）]	18（81.82）	15（60.00）	2.664	0.103
高脂血症[例（%）]	15（68.18）	13（52.00）	1.272	0.259
吸烟史[例（%）]	12（54.55）	8（32.00）	2.433	0.119
病灶侧（右/左）	17/5	13/12	3.237	0.072
NIHSS评分（分，Mean±SD）	2.23±1.23	2.44±1.26	-0.583	0.563
关键部位病灶[例（%）]	16（72.73）	6（24.00）	11.159	0.001
梗死病灶体积[mL，M（P₂₅，P₇₅）]	1.71（0.90，2.33）	1.28（0.90，1.45）	-1.771	0.077
MoCA评分[分，M（P₂₅，P₇₅）]
治疗前	18（17，21）	20（19，23）	-1.881	0.060
治疗后6个月	23（19，24）	28（27，29）	-5.892	＜0.001
MMSE评分[分，M（P₂₅，P₇₅）]
治疗前	23（19，24）	22（21，24）	-1.434	0.152
治疗后6个月	23（20，25）	28（27，30）	-4.907	＜0.001

项目	PSCI组（n=22）	N-PSCI组（n=25）	t/χ²/U值	P值
年龄（岁，Mean±SD）	63.73±3.69	62.56±4.70	0.937	0.354
性别（男/女）	13/9	11/14	1.066	0.302
受教育年限（年，Mean±SD）	9.55±0.86	9.96±1.14	-1.396	0.169
高血压病[例（%）]	16（72.73）	15（60.00）	0.844	0.358
糖尿病[例（%）]	18（81.82）	15（60.00）	2.664	0.103
高脂血症[例（%）]	15（68.18）	13（52.00）	1.272	0.259
吸烟史[例（%）]	12（54.55）	8（32.00）	2.433	0.119
病灶侧（右/左）	17/5	13/12	3.237	0.072
NIHSS评分（分，Mean±SD）	2.23±1.23	2.44±1.26	-0.583	0.563
关键部位病灶[例（%）]	16（72.73）	6（24.00）	11.159	0.001
梗死病灶体积[mL，M（P₂₅，P₇₅）]	1.71（0.90，2.33）	1.28（0.90，1.45）	-1.771	0.077
MoCA评分[分，M（P₂₅，P₇₅）]
治疗前	18（17，21）	20（19，23）	-1.881	0.060
治疗后6个月	23（19，24）	28（27，29）	-5.892	＜0.001
MMSE评分[分，M（P₂₅，P₇₅）]
治疗前	23（19，24）	22（21，24）	-1.434	0.152
治疗后6个月	23（20，25）	28（27，30）	-4.907	＜0.001

白质纤维束	簇体积(mm³)	峰值体素MNI坐标			差异	P值
白质纤维束	簇体积(mm³)	x	y	z	差异	P值
治疗前PSCI vs N-PSCI
FA
右SLF（外囊）	230	29	-5	18	N-PSCI＞PSCI	0.040
治疗后6个月PSCI vs N-PSCI
FA
右SLF	307	28	-5	27	N-PSCI＞PSCI	0.016
左ATR	410	-26	-6	26	N-PSCI＞PSCI	0.016
左IFOF	133	-25	32	-1	N-PSCI＞PSCI	0.016
左SLF	283	-36	-42	32	N-PSCI＞PSCI	0.017
左CST	82	-26	-23	14	N-PSCI＞PSCI	0.018
右CST	85	21	-31	49	N-PSCI＞PSCI	0.018
胼胝体	178	15	25	20	N-PSCI＞PSCI	0.020
MD
左SLF	278	-31	-20	36	PSCI＞N-PSCI	0.024
左CST	829	-26	-18	23	PSCI＞N-PSCI	0.026
PSCI组内的纵向差异
FA
左CST	305	-8	-20	-32	治疗前＞治疗后6个月	0.010
右SLF（外囊）	60	50	-2	17	治疗前＞治疗后6个月	0.010
右ATR	58	9	-46	-33	治疗前＞治疗后6个月	0.010
胼胝体	2010	8	15	20	治疗前＞治疗后6个月	0.034
MD
右SLF（外囊）	3008	34	-9	8	治疗后6个月＞治疗前	0.007
左ATR	354	-14	-51	-20	治疗后6个月＞治疗前	0.016
左CST	121	-18	-30	-36	治疗后6个月＞治疗前	0.016
N-PSCI组内的纵向差异
FA
左CST	475	-22	-40	-36	治疗前＞治疗后6个月	0.034
右CST	2840	20	-23	50	治疗前＞治疗后6个月	0.036
左SLF	605	-18	-20	45	治疗前＞治疗后6个月	0.038
右ATR	85	9	-38	-36	治疗前＞治疗后6个月	0.040
MD
左CST	73	-21	-58	-30	治疗后6个月＞治疗前	0.024
右CST	127	18	-58	-28	治疗后6个月＞治疗前	0.024
左SLF	1487	-33	-17	25	治疗后6个月＞治疗前	0.022
右IFOF（外囊）	890	30	10	8	治疗后6个月＞治疗前	0.022

白质纤维束	簇体积(mm³)	峰值体素MNI坐标			差异	P值
白质纤维束	簇体积(mm³)	x	y	z	差异	P值
治疗前PSCI vs N-PSCI
FA
右SLF（外囊）	230	29	-5	18	N-PSCI＞PSCI	0.040
治疗后6个月PSCI vs N-PSCI
FA
右SLF	307	28	-5	27	N-PSCI＞PSCI	0.016
左ATR	410	-26	-6	26	N-PSCI＞PSCI	0.016
左IFOF	133	-25	32	-1	N-PSCI＞PSCI	0.016
左SLF	283	-36	-42	32	N-PSCI＞PSCI	0.017
左CST	82	-26	-23	14	N-PSCI＞PSCI	0.018
右CST	85	21	-31	49	N-PSCI＞PSCI	0.018
胼胝体	178	15	25	20	N-PSCI＞PSCI	0.020
MD
左SLF	278	-31	-20	36	PSCI＞N-PSCI	0.024
左CST	829	-26	-18	23	PSCI＞N-PSCI	0.026
PSCI组内的纵向差异
FA
左CST	305	-8	-20	-32	治疗前＞治疗后6个月	0.010
右SLF（外囊）	60	50	-2	17	治疗前＞治疗后6个月	0.010
右ATR	58	9	-46	-33	治疗前＞治疗后6个月	0.010
胼胝体	2010	8	15	20	治疗前＞治疗后6个月	0.034
MD
右SLF（外囊）	3008	34	-9	8	治疗后6个月＞治疗前	0.007
左ATR	354	-14	-51	-20	治疗后6个月＞治疗前	0.016
左CST	121	-18	-30	-36	治疗后6个月＞治疗前	0.016
N-PSCI组内的纵向差异
FA
左CST	475	-22	-40	-36	治疗前＞治疗后6个月	0.034
右CST	2840	20	-23	50	治疗前＞治疗后6个月	0.036
左SLF	605	-18	-20	45	治疗前＞治疗后6个月	0.038
右ATR	85	9	-38	-36	治疗前＞治疗后6个月	0.040
MD
左CST	73	-21	-58	-30	治疗后6个月＞治疗前	0.024
右CST	127	18	-58	-28	治疗后6个月＞治疗前	0.024
左SLF	1487	-33	-17	25	治疗后6个月＞治疗前	0.022
右IFOF（外囊）	890	30	10	8	治疗后6个月＞治疗前	0.022

Please choose a citation manager

Content to export