Multiple sclerosis optic neuritis and trans-synaptic pathology on cortical thinning in people with multiple sclerosis

Ranjani Ganapathy Subramanian; Robert Zivadinov; Niels Bergsland; Michael G. Dwyer; Bianca Weinstock-Guttman; Dejan Jakimovski

doi:10.1007/s00415-023-11709-y

Multiple sclerosis optic neuritis and trans-synaptic pathology on cortical thinning in people with multiple sclerosis

Neurology

SUNY Buffalo

Research output: Contribution to journal › Article › peer-review

8 Scopus citations

Abstract

Background: The multi-order visual system represents an excellent testing site regarding the process of trans-synaptic degeneration. The presence and extent of global versus trans-synaptic neurodegeneration in people with multiple sclerosis (pwMS) is not clear. Objective: To explore cross-sectional and longitudinal relationships between retinal, thalamic and cortical changes in pwMS with and without MS-related optic neuritis (pwMSON and pwoMSON) using MRI and optical coherence tomography (OCT). Methods: 162 pwMS and 47 healthy controls (HCs) underwent OCT and brain MRI at baseline and 5.5-years follow-up. Peripapillary retinal nerve fiber layer (pRNFL) and macular ganglion cell inner plexiform layer (mGCIPL) thicknesses were determined. Global volume measures of brain parenchymal volume (BPV)/percent brain volume change (PBVC), thalamic volume and T2-lesion volume (LV) were derived using standard analysis protocols. Regional cortical thickness was determined using FreeSurfer. Cross-sectional and longitudinal relationship between the retinal measures, thalamic volume and cortical thickness were assessed using age, BPV/PBVC and T2-LV adjusted correlations and regressions. Results: After age, BPV and T2-LV adjustment, the thalamic volume explained additional variance in the thickness of pericalcarine (R² increase of 0.066, standardized β = 0.299, p = 0.039) and lateral occipital (R2 increase of 0.024, standardized β = 0.299, p = 0.039) gyrii in pwMSON. In pwoMSON, the thalamic volume was a significant predictor only of control (frontal) regions of pars opercularis. There was no relationship between thalamic atrophy and cortical thinning over the follow-up in both pwMS with and without MSON. While numerically lower in the pwMSON group, the inter-eye difference was not able to predict the presence of MSON. Conclusions: MSON can induce a measurable amount of trans-synaptic pathology on second-order cortical regions.

Original language	English
Pages (from-to)	3758-3769
Number of pages	12
Journal	Journal of Neurology
Volume	270
Issue number	8
DOIs	https://doi.org/10.1007/s00415-023-11709-y
State	Published - Aug 2023

Keywords

Ganglion cell and inner plexiform layers
Magnetic resonance imaging
Multiple sclerosis
Multiple sclerosis optic neuritis
Optical coherence tomography
Retinal nerve fiber layer

Access to Document

10.1007/s00415-023-11709-y

Cite this

@article{ac87520d1bd94f57abad88abcdc67619,

title = "Multiple sclerosis optic neuritis and trans-synaptic pathology on cortical thinning in people with multiple sclerosis",

abstract = "Background: The multi-order visual system represents an excellent testing site regarding the process of trans-synaptic degeneration. The presence and extent of global versus trans-synaptic neurodegeneration in people with multiple sclerosis (pwMS) is not clear. Objective: To explore cross-sectional and longitudinal relationships between retinal, thalamic and cortical changes in pwMS with and without MS-related optic neuritis (pwMSON and pwoMSON) using MRI and optical coherence tomography (OCT). Methods: 162 pwMS and 47 healthy controls (HCs) underwent OCT and brain MRI at baseline and 5.5-years follow-up. Peripapillary retinal nerve fiber layer (pRNFL) and macular ganglion cell inner plexiform layer (mGCIPL) thicknesses were determined. Global volume measures of brain parenchymal volume (BPV)/percent brain volume change (PBVC), thalamic volume and T2-lesion volume (LV) were derived using standard analysis protocols. Regional cortical thickness was determined using FreeSurfer. Cross-sectional and longitudinal relationship between the retinal measures, thalamic volume and cortical thickness were assessed using age, BPV/PBVC and T2-LV adjusted correlations and regressions. Results: After age, BPV and T2-LV adjustment, the thalamic volume explained additional variance in the thickness of pericalcarine (R2 increase of 0.066, standardized β = 0.299, p = 0.039) and lateral occipital (R2 increase of 0.024, standardized β = 0.299, p = 0.039) gyrii in pwMSON. In pwoMSON, the thalamic volume was a significant predictor only of control (frontal) regions of pars opercularis. There was no relationship between thalamic atrophy and cortical thinning over the follow-up in both pwMS with and without MSON. While numerically lower in the pwMSON group, the inter-eye difference was not able to predict the presence of MSON. Conclusions: MSON can induce a measurable amount of trans-synaptic pathology on second-order cortical regions.",

keywords = "Ganglion cell and inner plexiform layers, Magnetic resonance imaging, Multiple sclerosis, Multiple sclerosis optic neuritis, Optical coherence tomography, Retinal nerve fiber layer",

author = "\{Ganapathy Subramanian\}, Ranjani and Robert Zivadinov and Niels Bergsland and Dwyer, \{Michael G.\} and Bianca Weinstock-Guttman and Dejan Jakimovski",

note = "Publisher Copyright: {\textcopyright} 2023, The Author(s), under exclusive licence to Springer-Verlag GmbH Germany.",

year = "2023",

month = aug,

doi = "10.1007/s00415-023-11709-y",

language = "English",

volume = "270",

pages = "3758--3769",

journal = "Journal of Neurology",

issn = "0340-5354",

publisher = "Springer Science and Business Media Deutschland GmbH",

number = "8",

}

TY - JOUR

T1 - Multiple sclerosis optic neuritis and trans-synaptic pathology on cortical thinning in people with multiple sclerosis

AU - Ganapathy Subramanian, Ranjani

AU - Zivadinov, Robert

AU - Bergsland, Niels

AU - Dwyer, Michael G.

AU - Weinstock-Guttman, Bianca

AU - Jakimovski, Dejan

PY - 2023/8

Y1 - 2023/8

N2 - Background: The multi-order visual system represents an excellent testing site regarding the process of trans-synaptic degeneration. The presence and extent of global versus trans-synaptic neurodegeneration in people with multiple sclerosis (pwMS) is not clear. Objective: To explore cross-sectional and longitudinal relationships between retinal, thalamic and cortical changes in pwMS with and without MS-related optic neuritis (pwMSON and pwoMSON) using MRI and optical coherence tomography (OCT). Methods: 162 pwMS and 47 healthy controls (HCs) underwent OCT and brain MRI at baseline and 5.5-years follow-up. Peripapillary retinal nerve fiber layer (pRNFL) and macular ganglion cell inner plexiform layer (mGCIPL) thicknesses were determined. Global volume measures of brain parenchymal volume (BPV)/percent brain volume change (PBVC), thalamic volume and T2-lesion volume (LV) were derived using standard analysis protocols. Regional cortical thickness was determined using FreeSurfer. Cross-sectional and longitudinal relationship between the retinal measures, thalamic volume and cortical thickness were assessed using age, BPV/PBVC and T2-LV adjusted correlations and regressions. Results: After age, BPV and T2-LV adjustment, the thalamic volume explained additional variance in the thickness of pericalcarine (R2 increase of 0.066, standardized β = 0.299, p = 0.039) and lateral occipital (R2 increase of 0.024, standardized β = 0.299, p = 0.039) gyrii in pwMSON. In pwoMSON, the thalamic volume was a significant predictor only of control (frontal) regions of pars opercularis. There was no relationship between thalamic atrophy and cortical thinning over the follow-up in both pwMS with and without MSON. While numerically lower in the pwMSON group, the inter-eye difference was not able to predict the presence of MSON. Conclusions: MSON can induce a measurable amount of trans-synaptic pathology on second-order cortical regions.

AB - Background: The multi-order visual system represents an excellent testing site regarding the process of trans-synaptic degeneration. The presence and extent of global versus trans-synaptic neurodegeneration in people with multiple sclerosis (pwMS) is not clear. Objective: To explore cross-sectional and longitudinal relationships between retinal, thalamic and cortical changes in pwMS with and without MS-related optic neuritis (pwMSON and pwoMSON) using MRI and optical coherence tomography (OCT). Methods: 162 pwMS and 47 healthy controls (HCs) underwent OCT and brain MRI at baseline and 5.5-years follow-up. Peripapillary retinal nerve fiber layer (pRNFL) and macular ganglion cell inner plexiform layer (mGCIPL) thicknesses were determined. Global volume measures of brain parenchymal volume (BPV)/percent brain volume change (PBVC), thalamic volume and T2-lesion volume (LV) were derived using standard analysis protocols. Regional cortical thickness was determined using FreeSurfer. Cross-sectional and longitudinal relationship between the retinal measures, thalamic volume and cortical thickness were assessed using age, BPV/PBVC and T2-LV adjusted correlations and regressions. Results: After age, BPV and T2-LV adjustment, the thalamic volume explained additional variance in the thickness of pericalcarine (R2 increase of 0.066, standardized β = 0.299, p = 0.039) and lateral occipital (R2 increase of 0.024, standardized β = 0.299, p = 0.039) gyrii in pwMSON. In pwoMSON, the thalamic volume was a significant predictor only of control (frontal) regions of pars opercularis. There was no relationship between thalamic atrophy and cortical thinning over the follow-up in both pwMS with and without MSON. While numerically lower in the pwMSON group, the inter-eye difference was not able to predict the presence of MSON. Conclusions: MSON can induce a measurable amount of trans-synaptic pathology on second-order cortical regions.

KW - Ganglion cell and inner plexiform layers

KW - Magnetic resonance imaging

KW - Multiple sclerosis

KW - Multiple sclerosis optic neuritis

KW - Optical coherence tomography

KW - Retinal nerve fiber layer

UR - https://www.scopus.com/pages/publications/85153110124

U2 - 10.1007/s00415-023-11709-y

DO - 10.1007/s00415-023-11709-y

M3 - Article

C2 - 37067590

AN - SCOPUS:85153110124

SN - 0340-5354

VL - 270

SP - 3758

EP - 3769

JO - Journal of Neurology

JF - Journal of Neurology

IS - 8

ER -

Multiple sclerosis optic neuritis and trans-synaptic pathology on cortical thinning in people with multiple sclerosis

Abstract

Keywords

Access to Document

Other files and links

Fingerprint

Cite this