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 |
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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. |
doi_str_mv | 10.1002/jnr.25035 |
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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.</description><identifier>ISSN: 0360-4012</identifier><identifier>EISSN: 1097-4547</identifier><identifier>DOI: 10.1002/jnr.25035</identifier><identifier>PMID: 35316545</identifier><language>eng</language><publisher>United States: Wiley Subscription Services, Inc</publisher><subject>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</subject><ispartof>Journal of neuroscience research, 2022-07, Vol.100 (7), p.1395-1412</ispartof><rights>2022 Wiley Periodicals LLC.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4195-c27a3e3269972978019968a586644b79005770dbf06b3b14801e5077ecf736ff3</citedby><cites>FETCH-LOGICAL-c4195-c27a3e3269972978019968a586644b79005770dbf06b3b14801e5077ecf736ff3</cites><orcidid>0000-0001-5277-3249 ; 0000-0002-5462-6725 ; 0000-0002-2294-4032 ; 0000-0002-8491-0698 ; 0000-0002-2034-2556 ; 0000-0002-9339-6950 ; 0000-0001-5028-218X ; 0000-0002-0950-1093 ; 0000-0002-1791-8032 ; 0000-0003-4276-6226</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Fjnr.25035$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fjnr.25035$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27903,27904,45553,45554</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35316545$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><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><title>Multimodal magnetic resonance imaging quantification of gray matter alterations in relapsing‐remitting multiple sclerosis and neuromyelitis optica spectrum disorder</title><title>Journal of neuroscience research</title><addtitle>J Neurosci Res</addtitle><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.</description><subject>Abnormalities</subject><subject>Adult</subject><subject>Age</subject><subject>Aged</subject><subject>Antibodies</subject><subject>Cerebellum</subject><subject>demyelination</subject><subject>Density</subject><subject>diffusion tensor imaging</subject><subject>Diffusion Tensor Imaging - methods</subject><subject>Dispersion</subject><subject>Female</subject><subject>Females</subject><subject>Gray Matter - diagnostic imaging</subject><subject>Gray Matter - pathology</subject><subject>Humans</subject><subject>Magnetic Resonance Imaging</subject><subject>Male</subject><subject>Males</subject><subject>Medical imaging</subject><subject>Middle Aged</subject><subject>Multiple sclerosis</subject><subject>Multiple Sclerosis - pathology</subject><subject>Multiple Sclerosis, Relapsing-Remitting - diagnostic imaging</subject><subject>Myelin</subject><subject>neurite orientation dispersion and density imaging</subject><subject>Neuroimaging</subject><subject>neuroinflammation</subject><subject>Neuromyelitis</subject><subject>Neuromyelitis Optica - diagnostic imaging</subject><subject>Neuromyelitis Optica - pathology</subject><subject>neuronal loss</subject><subject>Resonance</subject><subject>Spatial analysis</subject><subject>Spatial distribution</subject><subject>Statistical analysis</subject><subject>Substantia grisea</subject><subject>synthetic magnetic resonance imaging</subject><subject>White Matter - pathology</subject><issn>0360-4012</issn><issn>1097-4547</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kU1uFDEQhS0EIkNgwQWQJTZk0Ynd_msvUQQBFEBCsG653dUjj9x2x3Yrmh1H4BQcjJPgyQQWSGxsqfy9V656CD2n5JwS0l7sQjpvBWHiAdpQolXDBVcP0YYwSRpOaHuCnuS8I4RoLdhjdMIEo1JwsUE_P66-uDmOxuPZbAMUZ3GCHIMJFrCrNRe2-GY1objJWVNcDDhOeJvMvipKgYSNr-fdS8YuVLk3S66yX99_JJhdKQeL-dBo8YCz9ZBidhmbMOIAa4rzHrwrtRKX2t_gvIAtaZ3x6HJMI6Sn6NFkfIZn9_cp-vb2zdfLd83156v3l6-vG8upFo1tlWHAWqm1arXqCNVadkZ0UnI-KE2IUIqMw0TkwAbKKwCCKAV2UkxOEztFr46-S4o3K-TSzy5b8N4EiGvuW8lbRrtOiIq-_AfdxTWF-rtKSdbRTsgDdXakbB05J5j6JdWlpn1PSX8Ir6_h9XfhVfbFveM6zDD-Jf-kVYGLI3DrPOz_79R_-PTlaPkbsy-oHA</recordid><startdate>202207</startdate><enddate>202207</enddate><creator>Andica, Christina</creator><creator>Hagiwara, Akifumi</creator><creator>Yokoyama, Kazumasa</creator><creator>Kato, Shimpei</creator><creator>Uchida, Wataru</creator><creator>Nishimura, Yuma</creator><creator>Fujita, Shohei</creator><creator>Kamagata, Koji</creator><creator>Hori, Masaaki</creator><creator>Tomizawa, Yuji</creator><creator>Hattori, Nobutaka</creator><creator>Aoki, Shigeki</creator><general>Wiley Subscription Services, Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7U7</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>K9.</scope><scope>P64</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-5277-3249</orcidid><orcidid>https://orcid.org/0000-0002-5462-6725</orcidid><orcidid>https://orcid.org/0000-0002-2294-4032</orcidid><orcidid>https://orcid.org/0000-0002-8491-0698</orcidid><orcidid>https://orcid.org/0000-0002-2034-2556</orcidid><orcidid>https://orcid.org/0000-0002-9339-6950</orcidid><orcidid>https://orcid.org/0000-0001-5028-218X</orcidid><orcidid>https://orcid.org/0000-0002-0950-1093</orcidid><orcidid>https://orcid.org/0000-0002-1791-8032</orcidid><orcidid>https://orcid.org/0000-0003-4276-6226</orcidid></search><sort><creationdate>202207</creationdate><title>Multimodal magnetic resonance imaging quantification of gray matter alterations in relapsing‐remitting multiple sclerosis and neuromyelitis optica spectrum disorder</title><author>Andica, Christina ; 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 & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Journal of neuroscience research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Andica, Christina</au><au>Hagiwara, Akifumi</au><au>Yokoyama, Kazumasa</au><au>Kato, Shimpei</au><au>Uchida, Wataru</au><au>Nishimura, Yuma</au><au>Fujita, Shohei</au><au>Kamagata, Koji</au><au>Hori, Masaaki</au><au>Tomizawa, Yuji</au><au>Hattori, Nobutaka</au><au>Aoki, Shigeki</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Multimodal magnetic resonance imaging quantification of gray matter alterations in relapsing‐remitting multiple sclerosis and neuromyelitis optica spectrum disorder</atitle><jtitle>Journal of neuroscience research</jtitle><addtitle>J Neurosci Res</addtitle><date>2022-07</date><risdate>2022</risdate><volume>100</volume><issue>7</issue><spage>1395</spage><epage>1412</epage><pages>1395-1412</pages><issn>0360-4012</issn><eissn>1097-4547</eissn><abstract>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.</abstract><cop>United States</cop><pub>Wiley Subscription Services, Inc</pub><pmid>35316545</pmid><doi>10.1002/jnr.25035</doi><tpages>18</tpages><orcidid>https://orcid.org/0000-0001-5277-3249</orcidid><orcidid>https://orcid.org/0000-0002-5462-6725</orcidid><orcidid>https://orcid.org/0000-0002-2294-4032</orcidid><orcidid>https://orcid.org/0000-0002-8491-0698</orcidid><orcidid>https://orcid.org/0000-0002-2034-2556</orcidid><orcidid>https://orcid.org/0000-0002-9339-6950</orcidid><orcidid>https://orcid.org/0000-0001-5028-218X</orcidid><orcidid>https://orcid.org/0000-0002-0950-1093</orcidid><orcidid>https://orcid.org/0000-0002-1791-8032</orcidid><orcidid>https://orcid.org/0000-0003-4276-6226</orcidid></addata></record> |
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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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