Mijntje M.I. Schellekens , Hao Li , Esther M. Boot , Jamie I. Verhoeven , Merel S. Ekker , Frederick J.A. Meijer , Roy P.C. Kessels , Frank-Erik de Leeuw , Anil M. Tuladhar
{"title":"White matter integrity and cognitive performance in the subacute phase after ischemic stroke in young adults","authors":"Mijntje M.I. Schellekens , Hao Li , Esther M. Boot , Jamie I. Verhoeven , Merel S. Ekker , Frederick J.A. Meijer , Roy P.C. Kessels , Frank-Erik de Leeuw , Anil M. Tuladhar","doi":"10.1016/j.nicl.2024.103711","DOIUrl":null,"url":null,"abstract":"<div><h3>Introduction</h3><div>Reduced white matter integrity outside the stroke lesion may be a potential contributor of post-stroke cognitive impairment. We aimed to investigate how a stroke lesion affects the integrity of surrounding white matter, and whether the integrity of the non-lesioned part of white matter tracts is associated with cognitive performance after ischemic stroke in young adults.</div></div><div><h3>Methods</h3><div>Patients from the ODYSSEY study, aged 18–49 years, with a first-ever ischemic stroke, underwent 3T MRI and cognitive assessment within six months after the index event. Using TractSeg and free water imaging, we analyzed free water corrected fractional anisotropy (FA<sub>T</sub>), free water corrected mean diffusivity (MD<sub>T</sub>), and free water (FW) of all white matter tracts outside the stroke lesion. We calculated FA<sub>T</sub> and FW in the lesioned white matter tracts at 2 mm incremental distances from the lesion, extending up to 10 mm, represented as Z-scores using the diffusion measures of controls. We categorized patients as no/mild or major vascular cognitive disorder (VCD) and compared with a stroke-free control group (n = 23). Group differences in diffusion measures were examined. We investigated associations between FA<sub>T</sub>, FW and cognitive performance across seven domains.</div></div><div><h3>Results</h3><div>Among 66 patients (median age 40.3 years (IQR 31.3–46.2); 54.5 % women), 22 had major VCD. In the different lesion expansions, we found differences in FA<sub>T</sub> (p = 0.009) and FW (p = 0.049). Patients with major VCD had lower FA<sub>T</sub> [range of Cohen’s d (0.65; 1.65)] and higher FW [Cohen’s d (−1.40; −0.64)] values compared to controls, both in the hemisphere affected by the lesion and the unaffected hemisphere. Performance in processing speed correlated with FA<sub>T</sub> across eight tracts in the affected hemisphere [range of R<sup>2</sup><sub>adj</sub> (0.30; 0.37)], and with FW in four tracts in the affected and three in the unaffected hemisphere [R<sup>2</sup><sub>adj</sub> (0.28; 0.38)].</div></div><div><h3>Discussion</h3><div>In the first months after a stroke, we observed a trend of microstructural changes remote from the lesion that diminish as the distance from the lesion increases. Tissue changes in the white matter outside the lesion are present in both hemispheres, but are more pronounced in the hemisphere affected by the stroke, and may contribute to worse cognitive performance.</div></div>","PeriodicalId":54359,"journal":{"name":"Neuroimage-Clinical","volume":"45 ","pages":"Article 103711"},"PeriodicalIF":3.4000,"publicationDate":"2024-11-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Neuroimage-Clinical","FirstCategoryId":"3","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S2213158224001529","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"NEUROIMAGING","Score":null,"Total":0}
引用次数: 0
Abstract
Introduction
Reduced white matter integrity outside the stroke lesion may be a potential contributor of post-stroke cognitive impairment. We aimed to investigate how a stroke lesion affects the integrity of surrounding white matter, and whether the integrity of the non-lesioned part of white matter tracts is associated with cognitive performance after ischemic stroke in young adults.
Methods
Patients from the ODYSSEY study, aged 18–49 years, with a first-ever ischemic stroke, underwent 3T MRI and cognitive assessment within six months after the index event. Using TractSeg and free water imaging, we analyzed free water corrected fractional anisotropy (FAT), free water corrected mean diffusivity (MDT), and free water (FW) of all white matter tracts outside the stroke lesion. We calculated FAT and FW in the lesioned white matter tracts at 2 mm incremental distances from the lesion, extending up to 10 mm, represented as Z-scores using the diffusion measures of controls. We categorized patients as no/mild or major vascular cognitive disorder (VCD) and compared with a stroke-free control group (n = 23). Group differences in diffusion measures were examined. We investigated associations between FAT, FW and cognitive performance across seven domains.
Results
Among 66 patients (median age 40.3 years (IQR 31.3–46.2); 54.5 % women), 22 had major VCD. In the different lesion expansions, we found differences in FAT (p = 0.009) and FW (p = 0.049). Patients with major VCD had lower FAT [range of Cohen’s d (0.65; 1.65)] and higher FW [Cohen’s d (−1.40; −0.64)] values compared to controls, both in the hemisphere affected by the lesion and the unaffected hemisphere. Performance in processing speed correlated with FAT across eight tracts in the affected hemisphere [range of R2adj (0.30; 0.37)], and with FW in four tracts in the affected and three in the unaffected hemisphere [R2adj (0.28; 0.38)].
Discussion
In the first months after a stroke, we observed a trend of microstructural changes remote from the lesion that diminish as the distance from the lesion increases. Tissue changes in the white matter outside the lesion are present in both hemispheres, but are more pronounced in the hemisphere affected by the stroke, and may contribute to worse cognitive performance.
期刊介绍:
NeuroImage: Clinical, a journal of diseases, disorders and syndromes involving the Nervous System, provides a vehicle for communicating important advances in the study of abnormal structure-function relationships of the human nervous system based on imaging.
The focus of NeuroImage: Clinical is on defining changes to the brain associated with primary neurologic and psychiatric diseases and disorders of the nervous system as well as behavioral syndromes and developmental conditions. The main criterion for judging papers is the extent of scientific advancement in the understanding of the pathophysiologic mechanisms of diseases and disorders, in identification of functional models that link clinical signs and symptoms with brain function and in the creation of image based tools applicable to a broad range of clinical needs including diagnosis, monitoring and tracking of illness, predicting therapeutic response and development of new treatments. Papers dealing with structure and function in animal models will also be considered if they reveal mechanisms that can be readily translated to human conditions.