Determinants of deep gray matter atrophy in multiple sclerosis: A multimodal MRI study

G. Pontillo, R. Lanzillo, C. Russo, M. D. Stasi, C. Paolella, E. A. Vola, C. Criscuolo, P. Borrelli, G. Palma, E. Tedeschi, X. V.B. Morra, X. A. Elefante, X. A. Brunetti, Sirio Cocozza

Research output: Contribution to journalArticle

Abstract

BACKGROUND AND PURPOSE: Deep gray matter involvement is a consistent feature in multiple sclerosis. The aim of this study was to evaluate the relationship between different deep gray matter alterations and the development of subcortical atrophy, as well as to investigate the possible different substrates of volume loss between phenotypes. MATERIALS AND METHODS: Seventy-seven patients with MS (52 with relapsing-remitting and 25 with progressive MS) and 41 healthy controls were enrolled in this cross-sectional study. MR imaging investigation included volumetric, DTI, PWI and Quantitative Susceptibility Mapping analyses. Deep gray matter structures were automatically segmented to obtain volumes and mean values for each MR imaging metric in the thalamus, caudate, putamen, and globus pallidus. Between-group differences were probed by ANCOVA analyses, while the contribution of different MR imaging metrics to deep gray matter atrophy was investigated via hierarchic multiple linear regression models. RESULTS: Patients with MS showed a multifaceted involvement of the thalamus and basal ganglia, with significant atrophy of all deep gray matter structures (P .001). In the relapsing-remitting MS group, WM lesion burden proved to be the main contributor to volume loss for all deep gray matter structures (P .006), with a minor role of local microstructural damage, which, in turn, was the main determinant of deep gray matter atrophy in patients with progressive MS (P .01), coupled with thalamic susceptibility changes (P .05). CONCLUSIONS: Our study confirms the diffuse involvement of deep gray matter in MS, demonstrating a different behavior between MS phenotypes, with subcortical GM atrophy mainly determined by global WM lesion burden in patients with relapsing-remitting MS, while local microstructural damage and susceptibility changes mainly accounted for the development of deep gray matter volume loss in patients with progressive MS.

Original languageEnglish
Pages (from-to)99-106
Number of pages8
JournalAmerican Journal of Neuroradiology
Volume40
Issue number1
DOIs
Publication statusE-pub ahead of print - Dec 20 2018

Fingerprint

Multiple Sclerosis
Atrophy
Thalamus
Linear Models
Phenotype
Gray Matter
Globus Pallidus
Putamen
Basal Ganglia
Cross-Sectional Studies

ASJC Scopus subject areas

  • Radiology Nuclear Medicine and imaging
  • Clinical Neurology

Cite this

Pontillo, G., Lanzillo, R., Russo, C., Stasi, M. D., Paolella, C., Vola, E. A., ... Cocozza, S. (2018). Determinants of deep gray matter atrophy in multiple sclerosis: A multimodal MRI study. American Journal of Neuroradiology, 40(1), 99-106. https://doi.org/10.3174/ajnr.A5915

Determinants of deep gray matter atrophy in multiple sclerosis : A multimodal MRI study. / Pontillo, G.; Lanzillo, R.; Russo, C.; Stasi, M. D.; Paolella, C.; Vola, E. A.; Criscuolo, C.; Borrelli, P.; Palma, G.; Tedeschi, E.; Morra, X. V.B.; Elefante, X. A.; Brunetti, X. A.; Cocozza, Sirio.

In: American Journal of Neuroradiology, Vol. 40, No. 1, 20.12.2018, p. 99-106.

Research output: Contribution to journalArticle

Pontillo, G, Lanzillo, R, Russo, C, Stasi, MD, Paolella, C, Vola, EA, Criscuolo, C, Borrelli, P, Palma, G, Tedeschi, E, Morra, XVB, Elefante, XA, Brunetti, XA & Cocozza, S 2018, 'Determinants of deep gray matter atrophy in multiple sclerosis: A multimodal MRI study', American Journal of Neuroradiology, vol. 40, no. 1, pp. 99-106. https://doi.org/10.3174/ajnr.A5915
Pontillo, G. ; Lanzillo, R. ; Russo, C. ; Stasi, M. D. ; Paolella, C. ; Vola, E. A. ; Criscuolo, C. ; Borrelli, P. ; Palma, G. ; Tedeschi, E. ; Morra, X. V.B. ; Elefante, X. A. ; Brunetti, X. A. ; Cocozza, Sirio. / Determinants of deep gray matter atrophy in multiple sclerosis : A multimodal MRI study. In: American Journal of Neuroradiology. 2018 ; Vol. 40, No. 1. pp. 99-106.
@article{d0c74841f91c4caa88858e3f23417f43,
title = "Determinants of deep gray matter atrophy in multiple sclerosis: A multimodal MRI study",
abstract = "BACKGROUND AND PURPOSE: Deep gray matter involvement is a consistent feature in multiple sclerosis. The aim of this study was to evaluate the relationship between different deep gray matter alterations and the development of subcortical atrophy, as well as to investigate the possible different substrates of volume loss between phenotypes. MATERIALS AND METHODS: Seventy-seven patients with MS (52 with relapsing-remitting and 25 with progressive MS) and 41 healthy controls were enrolled in this cross-sectional study. MR imaging investigation included volumetric, DTI, PWI and Quantitative Susceptibility Mapping analyses. Deep gray matter structures were automatically segmented to obtain volumes and mean values for each MR imaging metric in the thalamus, caudate, putamen, and globus pallidus. Between-group differences were probed by ANCOVA analyses, while the contribution of different MR imaging metrics to deep gray matter atrophy was investigated via hierarchic multiple linear regression models. RESULTS: Patients with MS showed a multifaceted involvement of the thalamus and basal ganglia, with significant atrophy of all deep gray matter structures (P .001). In the relapsing-remitting MS group, WM lesion burden proved to be the main contributor to volume loss for all deep gray matter structures (P .006), with a minor role of local microstructural damage, which, in turn, was the main determinant of deep gray matter atrophy in patients with progressive MS (P .01), coupled with thalamic susceptibility changes (P .05). CONCLUSIONS: Our study confirms the diffuse involvement of deep gray matter in MS, demonstrating a different behavior between MS phenotypes, with subcortical GM atrophy mainly determined by global WM lesion burden in patients with relapsing-remitting MS, while local microstructural damage and susceptibility changes mainly accounted for the development of deep gray matter volume loss in patients with progressive MS.",
author = "G. Pontillo and R. Lanzillo and C. Russo and Stasi, {M. D.} and C. Paolella and Vola, {E. A.} and C. Criscuolo and P. Borrelli and G. Palma and E. Tedeschi and Morra, {X. V.B.} and Elefante, {X. A.} and Brunetti, {X. A.} and Sirio Cocozza",
year = "2018",
month = "12",
day = "20",
doi = "10.3174/ajnr.A5915",
language = "English",
volume = "40",
pages = "99--106",
journal = "American Journal of Neuroradiology",
issn = "0195-6108",
publisher = "American Society of Neuroradiology",
number = "1",

}

TY - JOUR

T1 - Determinants of deep gray matter atrophy in multiple sclerosis

T2 - A multimodal MRI study

AU - Pontillo, G.

AU - Lanzillo, R.

AU - Russo, C.

AU - Stasi, M. D.

AU - Paolella, C.

AU - Vola, E. A.

AU - Criscuolo, C.

AU - Borrelli, P.

AU - Palma, G.

AU - Tedeschi, E.

AU - Morra, X. V.B.

AU - Elefante, X. A.

AU - Brunetti, X. A.

AU - Cocozza, Sirio

PY - 2018/12/20

Y1 - 2018/12/20

N2 - BACKGROUND AND PURPOSE: Deep gray matter involvement is a consistent feature in multiple sclerosis. The aim of this study was to evaluate the relationship between different deep gray matter alterations and the development of subcortical atrophy, as well as to investigate the possible different substrates of volume loss between phenotypes. MATERIALS AND METHODS: Seventy-seven patients with MS (52 with relapsing-remitting and 25 with progressive MS) and 41 healthy controls were enrolled in this cross-sectional study. MR imaging investigation included volumetric, DTI, PWI and Quantitative Susceptibility Mapping analyses. Deep gray matter structures were automatically segmented to obtain volumes and mean values for each MR imaging metric in the thalamus, caudate, putamen, and globus pallidus. Between-group differences were probed by ANCOVA analyses, while the contribution of different MR imaging metrics to deep gray matter atrophy was investigated via hierarchic multiple linear regression models. RESULTS: Patients with MS showed a multifaceted involvement of the thalamus and basal ganglia, with significant atrophy of all deep gray matter structures (P .001). In the relapsing-remitting MS group, WM lesion burden proved to be the main contributor to volume loss for all deep gray matter structures (P .006), with a minor role of local microstructural damage, which, in turn, was the main determinant of deep gray matter atrophy in patients with progressive MS (P .01), coupled with thalamic susceptibility changes (P .05). CONCLUSIONS: Our study confirms the diffuse involvement of deep gray matter in MS, demonstrating a different behavior between MS phenotypes, with subcortical GM atrophy mainly determined by global WM lesion burden in patients with relapsing-remitting MS, while local microstructural damage and susceptibility changes mainly accounted for the development of deep gray matter volume loss in patients with progressive MS.

AB - BACKGROUND AND PURPOSE: Deep gray matter involvement is a consistent feature in multiple sclerosis. The aim of this study was to evaluate the relationship between different deep gray matter alterations and the development of subcortical atrophy, as well as to investigate the possible different substrates of volume loss between phenotypes. MATERIALS AND METHODS: Seventy-seven patients with MS (52 with relapsing-remitting and 25 with progressive MS) and 41 healthy controls were enrolled in this cross-sectional study. MR imaging investigation included volumetric, DTI, PWI and Quantitative Susceptibility Mapping analyses. Deep gray matter structures were automatically segmented to obtain volumes and mean values for each MR imaging metric in the thalamus, caudate, putamen, and globus pallidus. Between-group differences were probed by ANCOVA analyses, while the contribution of different MR imaging metrics to deep gray matter atrophy was investigated via hierarchic multiple linear regression models. RESULTS: Patients with MS showed a multifaceted involvement of the thalamus and basal ganglia, with significant atrophy of all deep gray matter structures (P .001). In the relapsing-remitting MS group, WM lesion burden proved to be the main contributor to volume loss for all deep gray matter structures (P .006), with a minor role of local microstructural damage, which, in turn, was the main determinant of deep gray matter atrophy in patients with progressive MS (P .01), coupled with thalamic susceptibility changes (P .05). CONCLUSIONS: Our study confirms the diffuse involvement of deep gray matter in MS, demonstrating a different behavior between MS phenotypes, with subcortical GM atrophy mainly determined by global WM lesion burden in patients with relapsing-remitting MS, while local microstructural damage and susceptibility changes mainly accounted for the development of deep gray matter volume loss in patients with progressive MS.

UR - http://www.scopus.com/inward/record.url?scp=85059900932&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85059900932&partnerID=8YFLogxK

U2 - 10.3174/ajnr.A5915

DO - 10.3174/ajnr.A5915

M3 - Article

C2 - 30573464

AN - SCOPUS:85059900932

VL - 40

SP - 99

EP - 106

JO - American Journal of Neuroradiology

JF - American Journal of Neuroradiology

SN - 0195-6108

IS - 1

ER -