UCL Institute of Neurology, Department of Neuroinflammation, NMR Research Unit, London, UK.
Brain. 2010 Mar;133(Pt 3):858-67. doi: 10.1093/brain/awp335. Epub 2010 Jan 31.
Multiple sclerosis is an inflammatory, degenerative disease of the central nervous system. The most obvious pathological change in multiple sclerosis is multifocal demyelination of the white matter, but grey matter demyelination may be of equal or even greater importance for its clinical manifestations. In order to assess the pathogenetic role of lesions in the grey and white matter, and to explore the association between demyelinated and non-lesional brain tissue, tools are needed to depict each of these tissue components accurately in vivo. Due to its sensitivity in detecting white matter lesions, T(2)-weighted magnetic resonance imaging at 1.5 T is important in the diagnosis of multiple sclerosis. However, magnetic resonance imaging at 1.5 T largely fails to detect grey matter lesions. In this study, we used T(2)-weighted magnetic resonance imaging at 9.4 T to detect grey matter lesions in fixed post-mortem multiple sclerosis motor cortex. Furthermore, we produced T(1), T(2) and magnetization transfer ratio maps, and correlated these indices with quantitative histology [neuronal density, intensity of immunostaining for myelin basic protein (reflecting myelin content) and phosphorylated neurofilament (reflecting axonal area)] using t-tests and multivariate regression. In 21 tissue samples, 28 cortical grey matter lesions were visible on both T(2)-weighted magnetic resonance imaging and sections immunostained for myelin basic protein, 15/28 being mixed white and grey matter and 11/28 subpial cortical grey matter lesions; 2/28 cortical grey matter lesions involved all layers of the cortex. Compared with non-lesional cortex, cortical grey matter lesions showed reduction of neuronal density (98/mm(2), SD = 34/mm(2;) versus 129/mm(2), SD = 44; P < 0.01), phosphorylated neurofilament (1/transmittance = 1.16; SD = 0.09 versus 1.24; SD = 0.1; P < 0.01) and magnetization transfer ratio (31.1 pu; SD = 11.9 versus 37.5 pu; SD = 8.7; P = 0.01), and an increase of T(2) (25.9; SD = 5 versus 22.6 ms; SD = 4.7; P < 0.01). Associations were detected between phosphorylated neurofilament and myelin basic protein (r = 0.58, P < 0.01), myelin basic protein and T(2) (r = -0.59, P < 0.01), and neuronal density and T(1) (r = -0.57, P < 0.01). All indices correlated with duration of tissue fixation, however, including the latter in the analysis did not fundamentally affect the associations described. Our data show that T(2)-weighted magnetic resonance imaging at 9.4 T enables detection of cortical grey matter lesion in post-mortem multiple sclerosis brain. The quantitative associations suggest that in cortical grey matter T(1) may be a predictor of neuronal density, and T(2) of myelin content (and-secondarily-axons). Successful translation of these results into in vivo studies using high field magnetic resonance imaging (e.g. 3 T and 7 T) will improve the assessment of cortical pathology and thereby have an impact on the diagnosis and natural history studies of patients with multiple sclerosis, as well as clinical trial designs for putative treatments to prevent cortical demyelination and neuronal loss.
多发性硬化症是一种中枢神经系统的炎症性、退行性疾病。多发性硬化症最明显的病理变化是白质的多灶性脱髓鞘,但灰质脱髓鞘对其临床表现可能具有同等甚至更大的重要性。为了评估病变在灰质和白质中的致病作用,并探讨脱髓鞘和非病变脑组织之间的关系,需要有工具来准确地在体内描绘这些组织成分。由于其在检测白质病变方面的敏感性,1.5T 的 T2 加权磁共振成像在多发性硬化症的诊断中很重要。然而,1.5T 的磁共振成像在很大程度上无法检测到灰质病变。在这项研究中,我们使用 9.4T 的 T2 加权磁共振成像来检测固定的死后多发性硬化症运动皮层中的灰质病变。此外,我们制作了 T1、T2 和磁化传递比图,并使用 t 检验和多元回归分析将这些指标与定量组织学(神经元密度、髓鞘碱性蛋白免疫染色强度(反映髓鞘含量)和磷酸化神经丝(反映轴突面积))相关联。在 21 个组织样本中,28 个皮质灰质病变在 T2 加权磁共振成像和髓鞘碱性蛋白免疫染色的切片上均可见,15/28 为混合白质和灰质病变,11/28 为皮质下灰质病变;2/28 个皮质灰质病变累及皮层的所有层。与非病变皮质相比,皮质灰质病变表现为神经元密度降低(98/mm2,SD=34/mm2;与 129/mm2,SD=44;P<0.01)、磷酸化神经丝减少(1/透射率=1.16;SD=0.09 与 1.24;SD=0.1;P<0.01)和磁化转移率降低(31.1pu;SD=11.9 与 37.5pu;SD=8.7;P=0.01),以及 T2 延长(25.9;SD=5 与 22.6ms;SD=4.7;P<0.01)。在磷酸化神经丝和髓鞘碱性蛋白之间(r=0.58,P<0.01)、髓鞘碱性蛋白和 T2 之间(r=-0.59,P<0.01)以及神经元密度和 T1 之间(r=-0.57,P<0.01)都检测到了相关性。所有指标都与组织固定时间相关,但包括后者在内的分析并没有从根本上影响所描述的相关性。我们的数据表明,9.4T 的 T2 加权磁共振成像能够在死后多发性硬化症大脑中检测到皮质灰质病变。定量相关性表明,在皮质灰质中,T1 可能是神经元密度的预测因子,而 T2 可能是髓鞘含量(以及其次是轴突)的预测因子。将这些结果成功转化为使用高磁场磁共振成像(例如 3T 和 7T)进行的体内研究,将改善对皮质病变的评估,从而对多发性硬化症患者的诊断和自然史研究以及潜在治疗方法的临床试验设计产生影响,以预防皮质脱髓鞘和神经元丢失。
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