Cortical lesions impact cognitive decline in multiple sclerosis via volume loss of nonlesional cortex

IF 4.4 2区医学 Q1 CLINICAL NEUROLOGY

Annals of Clinical and Translational Neurology Pub Date : 2024-12-27 DOI:10.1002/acn3.52261

Eva A. Krijnen, Maureen van Dam, Albulena Bajrami, Piet M. Bouman, Samantha Noteboom, Frederik Barkhof, Bernard M.J. Uitdehaag, Martijn D. Steenwijk, Eric C. Klawiter, Ismail Koubiyr, Menno M. Schoonheim

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Abstract

Objective

To assess the interrelationship between cortical lesions and cortical thinning and volume loss in people with multiple sclerosis within cortical networks, and how this relates to future cognition.

Methods

In this longitudinal study, 230 people with multiple sclerosis and 60 healthy controls underwent 3 Tesla MRI at baseline and neuropsychological assessment at baseline and 5-year follow-up. Cortical regions (N = 212) were divided into seven functional networks. Regions were defined as either lesional or normal-appearing cortex based on presence of a cortical lesion on artificial intelligence-generated double inversion-recovery scans. Cortical volume and thickness were determined within lesional or normal-appearing cortex.

Results

Prevalence of at least one cortical lesion was highest in the limbic (73%) followed by the default mode network (70.9%). Multiple sclerosis-related cortical thinning was more pronounced in lesional (mean Z-score = 0.70 ± 0.84) compared to normal-appearing cortex (−0.45 ± 0.60; P < 0.001) in all, except sensorimotor, networks. Cognitive dysfunction, particularly of verbal memory, visuospatial memory, and inhibition, at follow-up was best predicted by baseline network volume of normal-appearing cortex of the default mode network [B (95% CI) = 0.31 (0.18; 0.43), P < 0.001]. Mediation analysis showed that the effect of cortical lesions on future cognition was mediated by volume loss of the normal-appearing instead of lesional cortex, independent of white matter lesion volume.

Interpretation

Multiple sclerosis-related cortical thinning was worse in lesional compared to normal-appearing cortex, while volume loss of normal-appearing cortex was most predictive of subsequent cognitive decline, particularly in the default mode network. Mediation analyses indicate that cortical lesions impact cognitive decline plausibly by inducing atrophy, rather than through a direct effect.

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皮质病变通过非病变皮质的体积损失影响多发性硬化症的认知能力下降。

目的：评估多发性硬化症患者皮质网络中皮质病变与皮质变薄和体积损失之间的相互关系，以及这与未来认知的关系。方法：在这项纵向研究中，230名多发性硬化症患者和60名健康对照者在基线时接受了3次特斯拉MRI检查，并在基线和5年随访时进行了神经心理学评估。皮质区（N = 212）分为7个功能网络。根据人工智能生成的双重反转恢复扫描中皮层病变的存在，将区域定义为病变或正常表现的皮层。在病变或正常表现的皮质内测定皮质体积和厚度。结果：至少一种皮层病变的患病率在边缘区最高（73%），其次是默认模式网络（70.9%）。多发性硬化症相关的皮层变薄在病变中更为明显（平均Z-score = 0.70±0.84），而在正常情况下(-0.45±0.60；解释：与正常表现的皮层相比，多发性硬化症相关的皮层变薄在病变中更严重，而正常表现的皮层体积损失最能预测随后的认知能力下降，特别是在默认模式网络中。调解分析表明，皮层损伤通过诱导萎缩而不是通过直接影响来影响认知能力下降。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

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来源期刊

Annals of Clinical and Translational Neurology Medicine-Neurology (clinical)

CiteScore

9.10

自引率

1.90%

发文量

218

审稿时长

8 weeks

期刊介绍： Annals of Clinical and Translational Neurology is a peer-reviewed journal for rapid dissemination of high-quality research related to all areas of neurology. The journal publishes original research and scholarly reviews focused on the mechanisms and treatments of diseases of the nervous system; high-impact topics in neurologic education; and other topics of interest to the clinical neuroscience community.