Loredana Storelli1, Ermelinda De Meo1,2, Lucia Moiola2, Maria Pia Amato3, Angelo Ghezzi4, Pierangelo Veggiotti5,6, Ruggero Capra7, Maria A. Rocca1,2, and Massimo Filippi1,2
1Neuroimaging Research Unit, Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan, Italy, 2Department of Neurology, Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan, Italy, 3Department NEUROFARBA, Section Neurosciences, University of Florence, Florence, Italy, 4Multiple Sclerosis Center, Ospedale di Gallarate, Gallarate, Italy, 5Department of Child Neurology and Psychiatry, C. Mondino National Neurological Institute, Pavia, Italy, 6Brain and Behaviour Department, University of Pavia, Pavia, Italy, 7Multiple Sclerosis Center, Spedali Civili of Brescia, Brescia, Italy
Synopsis
Despite widely recognized in pediatric
population with multiple sclerosis (MS), the pathogenesis of thalamic damage
remains largely unknown. This study was performed to explore the
microstructural abnormalities within this structure through the use of
quantitative MRI metrics (diffusion tensor, T1/T2-weighted ratio) considering the two different
thalamic interfaces (cerebrospinal fluid/thalamus and thalamus/white matter) as
sites of two different pathogenic processes: the first one accounting for cerebrospinal
fluid-mediated factor damage and the second one for diffuse neurodegenerative
damage. The study demonstrated an heterogeneous pathogenesis for thalamic
damage since the beginning of the disease.
Introduction
Both local
inflammatory demyelination and changes secondary to axonal transection of
fibers passing through focal white matter (WM) lesions can account for thalamic
abnormalities in multiple sclerosis (MS) patients.1 The thalamus
plays a major role in brain functioning, integrating inputs originating from
the cortex and subcortical structures. As a consequence, thalamic damage has
been related to clinical disability and cognitive impairment.2 Assessing
location of microstructural abnormalities within the thalamus as a function of
distance from cerebrospinal fluid (CSF) in pediatric MS patients could help to
identify whether at the beginning of disease, thalamic damage is due to CSF-mediated factors or thalamic neurodegeneration associated with
macroscopic damage. The aim of this study is to investigate, in-vivo,
pathological mechanisms underlying microstructural thalamic damage in pediatric
MS patients by applying quantitative MRI techniques.Methods
Sixty-eight pediatric
MS patients and 24 age and sex-matched healthy controls (HC) underwent 3T MRI
and clinical evaluation. As quantitative MRI metrics, we assessed diffusion
tensor (DT) imaging measures such as fractional anisotropy (FA) and mean
diffusivity (MD). In addition, T1/T2-weighted ratio maps were estimated using
an in-house implemented method (Matlab®) adapted from Ganzetti et al.3
We tested for: differences
in thalamic volume (estimated with FIRST tool from FSL library), and
quantitative DT and T1/T2-weighted ratio MRI measures both globally and
within concentric bands originating from CSF/thalamus interface (as a function
of the geodesic distance of the thalamus from the CSF, Figure 1). Moreover, we
assessed the relation between thalamic, cortical, and WM metrics, and the
contribution of MRI metrics to clinical disability.Results
Compared to HC,
pediatric MS patients had reduced thalamic FA (p=0.009) and no thalamic atrophy.
In pediatric MS, significant reduction of FA was observed in bands nearest to
CSF and in those nearest to WM compared to HC (Figure 2). Significant
abnormalities of MD and T1/T2-weighted ratio were respectively observed in
thalamic regions next to CSF and to WM (Figure 3). Global and regional FA
abnormalities as well as T1/T2-weighted ratio abnormalities showed significant
correlations with disease duration, while MD alterations showed significant
correlations with cortical thinning. No significant correlations between
thalamic damage and T2 lesion volumes or clinical disability were observed.Discussion
This study demonstrated a heterogeneous
pathogenesis for thalamic damage since the beginning of the disease, accounting
for both cerebrospinal fluid mediated and diffuse normal appearing WM damage.Conclusions
The abnormalities
observed suggest that thalamic damage occurs from the earliest stages of MS and
is determined by heterogeneous pathological processes, individuating the thalamus as a critical
barometer of diffuse neuronal pathology in MS.Acknowledgements
Partially supported by grants from Italian Ministry of
Health (GR-2009-1529671) and Fondazione Italiana Sclerosi Multipla (FISM2016/R/23).References
1. Louapre C., Govindarajan S.T., Giannì C., et al., Heterogeneous pathological processes account for thalamic
degeneration in multiple sclerosis:
Insights from 7 T imaging.
Mult Scler. 2018 Oct;24(11):1433-1444.
2.
Till C., Ho C., Dudani A. et al., Magnetic resonance
imaging predictors of executive functioning in patients with pediatric-onset
multiple sclerosis. Archives of clinical
neuropsychology; 2012, 27(5), 495-509.
3. Ganzetti M., Wenderoth N., Mantini D., Whole brain
myelin mapping using T1- and T2- weighted MR imaging data. Front Hum Neurosci., 2014, 8: 671.