Multimodal magnetic resonance imaging quantification of gray matter alterations in relapsing‐remitting multiple sclerosis and neuromyelitis optica spectrum disorder

Herein, we combined neurite orientation dispersion and density imaging (NODDI) and synthetic magnetic resonance imaging (SyMRI) to evaluate the spatial distribution and extent of gray matter (GM) microstructural alterations in patients with relapsing‐remitting multiple sclerosis (RRMS) and neuromyel...

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Veröffentlicht in:Journal of neuroscience research 2022-07, Vol.100 (7), p.1395-1412
Hauptverfasser: Andica, Christina, Hagiwara, Akifumi, Yokoyama, Kazumasa, Kato, Shimpei, Uchida, Wataru, Nishimura, Yuma, Fujita, Shohei, Kamagata, Koji, Hori, Masaaki, Tomizawa, Yuji, Hattori, Nobutaka, Aoki, Shigeki
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container_issue 7
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container_title Journal of neuroscience research
container_volume 100
creator Andica, Christina
Hagiwara, Akifumi
Yokoyama, Kazumasa
Kato, Shimpei
Uchida, Wataru
Nishimura, Yuma
Fujita, Shohei
Kamagata, Koji
Hori, Masaaki
Tomizawa, Yuji
Hattori, Nobutaka
Aoki, Shigeki
description Herein, we combined neurite orientation dispersion and density imaging (NODDI) and synthetic magnetic resonance imaging (SyMRI) to evaluate the spatial distribution and extent of gray matter (GM) microstructural alterations in patients with relapsing‐remitting multiple sclerosis (RRMS) and neuromyelitis optica spectrum disorder (NMOSD). The NODDI (neurite density index [NDI], orientation dispersion index [ODI], and isotropic volume fraction [ISOVF]) and SyMRI (myelin volume fraction [MVF]) measures were compared between age‐ and sex‐matched groups of 30 patients with RRMS (6 males and 24 females; mean age, 51.43 ± 8.02 years), 18 patients with anti‐aquaporin‐4 antibody‐positive NMOSD (2 males and 16 females; mean age, 52.67 ± 16.07 years), and 19 healthy controls (6 males and 13 females; mean age, 51.47 ± 9.25 years) using GM‐based spatial statistical analysis. Patients with RRMS showed reduced NDI and MVF and increased ODI and ISOVF, predominantly in the limbic and paralimbic regions, when compared with healthy controls, while only increases in ODI and ISOVF were observed when compared with NMOSD. Compared to NDI and MVF, the changes in ODI and ISOVF were observed more widely, including in the cerebellar cortex. These abnormalities were associated with disease progression and disability. In contrast, patients with NMOSD only showed reduced NDI mainly in the cerebellar, limbic, and paralimbic cortices when compared with healthy controls and patients with RRMS. Taken together, our study supports the notion that GM pathologies in RRMS are distinct from those of NMOSD. However, owing to the limitations of the study, the results should be cautiously interpreted. Using neurite orientation dispersion and density imaging and synthetic magnetic resonance imaging‐derived myelin volume fraction, we showed gray matter alterations in patients with relapsing‐remitting multiple sclerosis (RRMS) and neuromyelitis optica spectrum disorder (NMOSD). Our findings suggested extensive neuroinflammation, along with a lesser extent demyelination and neuronal loss in RRMS. In contrast, we observed substantial neuronal loss with no evidence of demyelination and neuroinflammation in NMOSD.
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The NODDI (neurite density index [NDI], orientation dispersion index [ODI], and isotropic volume fraction [ISOVF]) and SyMRI (myelin volume fraction [MVF]) measures were compared between age‐ and sex‐matched groups of 30 patients with RRMS (6 males and 24 females; mean age, 51.43 ± 8.02 years), 18 patients with anti‐aquaporin‐4 antibody‐positive NMOSD (2 males and 16 females; mean age, 52.67 ± 16.07 years), and 19 healthy controls (6 males and 13 females; mean age, 51.47 ± 9.25 years) using GM‐based spatial statistical analysis. Patients with RRMS showed reduced NDI and MVF and increased ODI and ISOVF, predominantly in the limbic and paralimbic regions, when compared with healthy controls, while only increases in ODI and ISOVF were observed when compared with NMOSD. Compared to NDI and MVF, the changes in ODI and ISOVF were observed more widely, including in the cerebellar cortex. These abnormalities were associated with disease progression and disability. 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The NODDI (neurite density index [NDI], orientation dispersion index [ODI], and isotropic volume fraction [ISOVF]) and SyMRI (myelin volume fraction [MVF]) measures were compared between age‐ and sex‐matched groups of 30 patients with RRMS (6 males and 24 females; mean age, 51.43 ± 8.02 years), 18 patients with anti‐aquaporin‐4 antibody‐positive NMOSD (2 males and 16 females; mean age, 52.67 ± 16.07 years), and 19 healthy controls (6 males and 13 females; mean age, 51.47 ± 9.25 years) using GM‐based spatial statistical analysis. Patients with RRMS showed reduced NDI and MVF and increased ODI and ISOVF, predominantly in the limbic and paralimbic regions, when compared with healthy controls, while only increases in ODI and ISOVF were observed when compared with NMOSD. Compared to NDI and MVF, the changes in ODI and ISOVF were observed more widely, including in the cerebellar cortex. These abnormalities were associated with disease progression and disability. 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Hagiwara, Akifumi ; Yokoyama, Kazumasa ; Kato, Shimpei ; Uchida, Wataru ; Nishimura, Yuma ; Fujita, Shohei ; Kamagata, Koji ; Hori, Masaaki ; Tomizawa, Yuji ; Hattori, Nobutaka ; Aoki, Shigeki</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4195-c27a3e3269972978019968a586644b79005770dbf06b3b14801e5077ecf736ff3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Abnormalities</topic><topic>Adult</topic><topic>Age</topic><topic>Aged</topic><topic>Antibodies</topic><topic>Cerebellum</topic><topic>demyelination</topic><topic>Density</topic><topic>diffusion tensor imaging</topic><topic>Diffusion Tensor Imaging - methods</topic><topic>Dispersion</topic><topic>Female</topic><topic>Females</topic><topic>Gray Matter - diagnostic imaging</topic><topic>Gray Matter - pathology</topic><topic>Humans</topic><topic>Magnetic Resonance Imaging</topic><topic>Male</topic><topic>Males</topic><topic>Medical imaging</topic><topic>Middle Aged</topic><topic>Multiple sclerosis</topic><topic>Multiple Sclerosis - pathology</topic><topic>Multiple Sclerosis, Relapsing-Remitting - diagnostic imaging</topic><topic>Myelin</topic><topic>neurite orientation dispersion and density imaging</topic><topic>Neuroimaging</topic><topic>neuroinflammation</topic><topic>Neuromyelitis</topic><topic>Neuromyelitis Optica - diagnostic imaging</topic><topic>Neuromyelitis Optica - pathology</topic><topic>neuronal loss</topic><topic>Resonance</topic><topic>Spatial analysis</topic><topic>Spatial distribution</topic><topic>Statistical analysis</topic><topic>Substantia grisea</topic><topic>synthetic magnetic resonance imaging</topic><topic>White Matter - pathology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Andica, Christina</creatorcontrib><creatorcontrib>Hagiwara, Akifumi</creatorcontrib><creatorcontrib>Yokoyama, Kazumasa</creatorcontrib><creatorcontrib>Kato, Shimpei</creatorcontrib><creatorcontrib>Uchida, Wataru</creatorcontrib><creatorcontrib>Nishimura, Yuma</creatorcontrib><creatorcontrib>Fujita, Shohei</creatorcontrib><creatorcontrib>Kamagata, Koji</creatorcontrib><creatorcontrib>Hori, Masaaki</creatorcontrib><creatorcontrib>Tomizawa, Yuji</creatorcontrib><creatorcontrib>Hattori, Nobutaka</creatorcontrib><creatorcontrib>Aoki, Shigeki</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Calcium &amp; 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The NODDI (neurite density index [NDI], orientation dispersion index [ODI], and isotropic volume fraction [ISOVF]) and SyMRI (myelin volume fraction [MVF]) measures were compared between age‐ and sex‐matched groups of 30 patients with RRMS (6 males and 24 females; mean age, 51.43 ± 8.02 years), 18 patients with anti‐aquaporin‐4 antibody‐positive NMOSD (2 males and 16 females; mean age, 52.67 ± 16.07 years), and 19 healthy controls (6 males and 13 females; mean age, 51.47 ± 9.25 years) using GM‐based spatial statistical analysis. Patients with RRMS showed reduced NDI and MVF and increased ODI and ISOVF, predominantly in the limbic and paralimbic regions, when compared with healthy controls, while only increases in ODI and ISOVF were observed when compared with NMOSD. Compared to NDI and MVF, the changes in ODI and ISOVF were observed more widely, including in the cerebellar cortex. These abnormalities were associated with disease progression and disability. In contrast, patients with NMOSD only showed reduced NDI mainly in the cerebellar, limbic, and paralimbic cortices when compared with healthy controls and patients with RRMS. Taken together, our study supports the notion that GM pathologies in RRMS are distinct from those of NMOSD. However, owing to the limitations of the study, the results should be cautiously interpreted. Using neurite orientation dispersion and density imaging and synthetic magnetic resonance imaging‐derived myelin volume fraction, we showed gray matter alterations in patients with relapsing‐remitting multiple sclerosis (RRMS) and neuromyelitis optica spectrum disorder (NMOSD). Our findings suggested extensive neuroinflammation, along with a lesser extent demyelination and neuronal loss in RRMS. 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subjects Abnormalities
Adult
Age
Aged
Antibodies
Cerebellum
demyelination
Density
diffusion tensor imaging
Diffusion Tensor Imaging - methods
Dispersion
Female
Females
Gray Matter - diagnostic imaging
Gray Matter - pathology
Humans
Magnetic Resonance Imaging
Male
Males
Medical imaging
Middle Aged
Multiple sclerosis
Multiple Sclerosis - pathology
Multiple Sclerosis, Relapsing-Remitting - diagnostic imaging
Myelin
neurite orientation dispersion and density imaging
Neuroimaging
neuroinflammation
Neuromyelitis
Neuromyelitis Optica - diagnostic imaging
Neuromyelitis Optica - pathology
neuronal loss
Resonance
Spatial analysis
Spatial distribution
Statistical analysis
Substantia grisea
synthetic magnetic resonance imaging
White Matter - pathology
title Multimodal magnetic resonance imaging quantification of gray matter alterations in relapsing‐remitting multiple sclerosis and neuromyelitis optica spectrum disorder
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