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. 2018 Jun 1;141(6):1665-1677.
doi: 10.1093/brain/awy088.

Progression of regional grey matter atrophy in multiple sclerosis

Affiliations

Progression of regional grey matter atrophy in multiple sclerosis

Arman Eshaghi et al. Brain. .

Abstract

See Stankoff and Louapre (doi:10.1093/brain/awy114) for a scientific commentary on this article.Grey matter atrophy is present from the earliest stages of multiple sclerosis, but its temporal ordering is poorly understood. We aimed to determine the sequence in which grey matter regions become atrophic in multiple sclerosis and its association with disability accumulation. In this longitudinal study, we included 1417 subjects: 253 with clinically isolated syndrome, 708 with relapsing-remitting multiple sclerosis, 128 with secondary-progressive multiple sclerosis, 125 with primary-progressive multiple sclerosis, and 203 healthy control subjects from seven European centres. Subjects underwent repeated MRI (total number of scans 3604); the mean follow-up for patients was 2.41 years (standard deviation = 1.97). Disability was scored using the Expanded Disability Status Scale. We calculated the volume of brain grey matter regions and brainstem using an unbiased within-subject template and used an established data-driven event-based model to determine the sequence of occurrence of atrophy and its uncertainty. We assigned each subject to a specific event-based model stage, based on the number of their atrophic regions. Linear mixed-effects models were used to explore associations between the rate of increase in event-based model stages, and T2 lesion load, disease-modifying treatments, comorbidity, disease duration and disability accumulation. The first regions to become atrophic in patients with clinically isolated syndrome and relapse-onset multiple sclerosis were the posterior cingulate cortex and precuneus, followed by the middle cingulate cortex, brainstem and thalamus. A similar sequence of atrophy was detected in primary-progressive multiple sclerosis with the involvement of the thalamus, cuneus, precuneus, and pallidum, followed by the brainstem and posterior cingulate cortex. The cerebellum, caudate and putamen showed early atrophy in relapse-onset multiple sclerosis and late atrophy in primary-progressive multiple sclerosis. Patients with secondary-progressive multiple sclerosis showed the highest event-based model stage (the highest number of atrophic regions, P < 0.001) at the study entry. All multiple sclerosis phenotypes, but clinically isolated syndrome, showed a faster rate of increase in the event-based model stage than healthy controls. T2 lesion load and disease duration in all patients were associated with increased event-based model stage, but no effects of disease-modifying treatments and comorbidity on event-based model stage were observed. The annualized rate of event-based model stage was associated with the disability accumulation in relapsing-remitting multiple sclerosis, independent of disease duration (P < 0.0001). The data-driven staging of atrophy progression in a large multiple sclerosis sample demonstrates that grey matter atrophy spreads to involve more regions over time. The sequence in which regions become atrophic is reasonably consistent across multiple sclerosis phenotypes. The spread of atrophy was associated with disease duration and with disability accumulation over time in relapsing-remitting multiple sclerosis.

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Figures

Figure 1
Figure 1
The event-based model steps to estimate the most likely sequence of atrophy progression. The three steps are: (A) adjusting for nuisance variables, and region selection; (B) calculating the best-fit probability distributions for normal and atrophic brain regions; searching for the most likely sequence; and (C) quantifying the uncertainty with cross-validation. [B(i)] The distribution of the volume in an example region in healthy controls and patients and the corresponding mixture model. (ii) The steps for greedy ascent search. (iii) A matrix showing a sequence of atrophy progression on the y-axis, and the position in the sequence of each region ranging from 1 to the total number of regions on the x-axis. The intensity of each matrix entry corresponds to the proportion of Markov Chain Monte Carlo samples of the posterior distribution where a certain region of y-axis appears at the respective stage of x-axis.
Figure 2
Figure 2
Comparisons of regional volumes between groups. Box plots at y-axis show z-scores of the corresponding region shown at x-axis. Lower and upper hinges of each boxplot correspond to 25th and 75th percentiles of data. We selected 24 regions that showed significant difference (P < 0.01 corrected) between all patients with multiple sclerosis and healthy controls at baseline visit. CIS = clinically isolated syndrome; HC = healthy control; PPMS = primary progressive multiple sclerosis; RRMS = relapsing-remitting multiple sclerosis; SPMS = secondary progressive multiple sclerosis.
Figure 3
Figure 3
Sequences of atrophy progression and patient staging. The positional variance diagrams for (A) relapse-onset multiple sclerosis, (B) primary-progressive multiple sclerosis (PPMS) and (C) merged cohort of patients, show the most likely sequences of atrophy and their associated uncertainty. In AC, the y-axis shows the most likely sequence of atrophy progression, and the x-axis shows the sequence position ranging from one to the total number of regions. The intensity of each rectangle corresponds to the proportion of Markov Chain Monte Carlo samples of the posterior distribution where a certain region of y-axis appears at the respective stage of the x-axis. (D) The evolution of the event-based model (EBM) stage (or atrophy progression staging) over time in clinically isolated syndrome and relapse-onset multiple sclerosis together and primary-progressive multiple sclerosis. Each line in D is the prediction of the mixed-effects model whose ribbon shows standard error of the prediction. MS = multiple sclerosis.
Figure 4
Figure 4
Regional atrophy and its sequence of progression in all grey matter regions plus brainstem in relapse-onset disease and primary progressive multiple sclerosis. The probability of atrophy in each region was calculated from the positional variance diagrams and colour coded, so that brighter colour corresponded to a higher probability of seeing atrophy in the corresponding event-based model stage. MS = multiple sclerosis.

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