Spinal cord and brain atrophy patterns in neuromyelitis optica spectrum disorder and multiple sclerosis
Background Spinal cord and brain atrophy are common in neuromyelitis optica spectrum disorder (NMOSD) and relapsing-remitting multiple sclerosis (RRMS) but harbor distinct patterns accounting for disability and cognitive impairment. Methods This study included 209 NMOSD and 304 RRMS patients and 436...
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Veröffentlicht in: | Journal of neurology 2024-06, Vol.271 (6), p.3595-3609 |
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creator | Hua, Tiantian Fan, Houyou Duan, Yunyun Tian, Decai Chen, Zhenpeng Xu, Xiaolu Bai, Yutong Li, Yuna Zhang, Ningnannan Sun, Jie Li, Haiqing Li, Yuxin Li, Yongmei Zeng, Chun Han, Xuemei Zhou, Fuqing Huang, Muhua Xu, Siyao Jin, Ying Li, Hongfang Zhuo, Zhizheng Zhang, Xinghu Liu, Yaou |
description | Background
Spinal cord and brain atrophy are common in neuromyelitis optica spectrum disorder (NMOSD) and relapsing-remitting multiple sclerosis (RRMS) but harbor distinct patterns accounting for disability and cognitive impairment.
Methods
This study included 209 NMOSD and 304 RRMS patients and 436 healthy controls. Non-negative matrix factorization was used to parse differences in spinal cord and brain atrophy at subject level into distinct patterns based on structural MRI. The weights of patterns were obtained using a linear regression model and associated with Expanded Disability Status Scale (EDSS) and cognitive scores. Additionally, patients were divided into cognitive impairment (CI) and cognitive preservation (CP) groups.
Results
Three patterns were observed in NMOSD: (1) Spinal Cord-Deep Grey Matter (SC-DGM) pattern was associated with high EDSS scores and decline of visuospatial memory function; (2) Frontal-Temporal pattern was associated with decline of language learning function; and (3) Cerebellum-Brainstem pattern had no observed association. Patients with CI had higher weights of SC-DGM pattern than CP group. Three patterns were observed in RRMS: (1) DGM pattern was associated with high EDSS scores, decreased information processing speed, and decreased language learning and visuospatial memory functions; (2) Frontal-Temporal pattern was associated with overall cognitive decline; and (3) Occipital pattern had no observed association. Patients with CI trended to have higher weights of DGM and Frontal-Temporal patterns than CP group.
Conclusion
This study estimated the heterogeneity of spinal cord and brain atrophy patterns in NMOSD and RRMS patients at individual level, and evaluated the clinical relevance of these patterns, which may contribute to stratifying participants for targeted therapy. |
doi_str_mv | 10.1007/s00415-024-12281-9 |
format | Article |
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Spinal cord and brain atrophy are common in neuromyelitis optica spectrum disorder (NMOSD) and relapsing-remitting multiple sclerosis (RRMS) but harbor distinct patterns accounting for disability and cognitive impairment.
Methods
This study included 209 NMOSD and 304 RRMS patients and 436 healthy controls. Non-negative matrix factorization was used to parse differences in spinal cord and brain atrophy at subject level into distinct patterns based on structural MRI. The weights of patterns were obtained using a linear regression model and associated with Expanded Disability Status Scale (EDSS) and cognitive scores. Additionally, patients were divided into cognitive impairment (CI) and cognitive preservation (CP) groups.
Results
Three patterns were observed in NMOSD: (1) Spinal Cord-Deep Grey Matter (SC-DGM) pattern was associated with high EDSS scores and decline of visuospatial memory function; (2) Frontal-Temporal pattern was associated with decline of language learning function; and (3) Cerebellum-Brainstem pattern had no observed association. Patients with CI had higher weights of SC-DGM pattern than CP group. Three patterns were observed in RRMS: (1) DGM pattern was associated with high EDSS scores, decreased information processing speed, and decreased language learning and visuospatial memory functions; (2) Frontal-Temporal pattern was associated with overall cognitive decline; and (3) Occipital pattern had no observed association. Patients with CI trended to have higher weights of DGM and Frontal-Temporal patterns than CP group.
Conclusion
This study estimated the heterogeneity of spinal cord and brain atrophy patterns in NMOSD and RRMS patients at individual level, and evaluated the clinical relevance of these patterns, which may contribute to stratifying participants for targeted therapy.</description><identifier>ISSN: 0340-5354</identifier><identifier>ISSN: 1432-1459</identifier><identifier>EISSN: 1432-1459</identifier><identifier>DOI: 10.1007/s00415-024-12281-9</identifier><identifier>PMID: 38558149</identifier><language>eng</language><publisher>Berlin/Heidelberg: Springer Berlin Heidelberg</publisher><subject>Adult ; Atrophy ; Atrophy - pathology ; Brain - diagnostic imaging ; Brain - pathology ; Brain stem ; Cerebellum ; Cognitive ability ; Cognitive Dysfunction - diagnostic imaging ; Cognitive Dysfunction - etiology ; Cognitive Dysfunction - pathology ; Cognitive Dysfunction - physiopathology ; Female ; Gray Matter - diagnostic imaging ; Gray Matter - pathology ; Humans ; Information processing ; Learning ; Magnetic Resonance Imaging ; Male ; Medicine ; Medicine & Public Health ; Memory ; Middle Aged ; Multiple sclerosis ; Multiple Sclerosis, Relapsing-Remitting - diagnostic imaging ; Multiple Sclerosis, Relapsing-Remitting - pathology ; Multiple Sclerosis, Relapsing-Remitting - physiopathology ; Neurology ; Neuromyelitis ; Neuromyelitis Optica - diagnostic imaging ; Neuromyelitis Optica - pathology ; Neuroradiology ; Neurosciences ; Original Communication ; Spatial memory ; Spinal cord ; Spinal Cord - diagnostic imaging ; Spinal Cord - pathology ; Substantia grisea</subject><ispartof>Journal of neurology, 2024-06, Vol.271 (6), p.3595-3609</ispartof><rights>The Author(s), under exclusive licence to Springer-Verlag GmbH Germany 2024. Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.</rights><rights>2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c326t-74dab5965ea030cb88495a89673cbf486bdfc63a06854bfcf9ff056a256252d63</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s00415-024-12281-9$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s00415-024-12281-9$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,776,780,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38558149$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Hua, Tiantian</creatorcontrib><creatorcontrib>Fan, Houyou</creatorcontrib><creatorcontrib>Duan, Yunyun</creatorcontrib><creatorcontrib>Tian, Decai</creatorcontrib><creatorcontrib>Chen, Zhenpeng</creatorcontrib><creatorcontrib>Xu, Xiaolu</creatorcontrib><creatorcontrib>Bai, Yutong</creatorcontrib><creatorcontrib>Li, Yuna</creatorcontrib><creatorcontrib>Zhang, Ningnannan</creatorcontrib><creatorcontrib>Sun, Jie</creatorcontrib><creatorcontrib>Li, Haiqing</creatorcontrib><creatorcontrib>Li, Yuxin</creatorcontrib><creatorcontrib>Li, Yongmei</creatorcontrib><creatorcontrib>Zeng, Chun</creatorcontrib><creatorcontrib>Han, Xuemei</creatorcontrib><creatorcontrib>Zhou, Fuqing</creatorcontrib><creatorcontrib>Huang, Muhua</creatorcontrib><creatorcontrib>Xu, Siyao</creatorcontrib><creatorcontrib>Jin, Ying</creatorcontrib><creatorcontrib>Li, Hongfang</creatorcontrib><creatorcontrib>Zhuo, Zhizheng</creatorcontrib><creatorcontrib>Zhang, Xinghu</creatorcontrib><creatorcontrib>Liu, Yaou</creatorcontrib><title>Spinal cord and brain atrophy patterns in neuromyelitis optica spectrum disorder and multiple sclerosis</title><title>Journal of neurology</title><addtitle>J Neurol</addtitle><addtitle>J Neurol</addtitle><description>Background
Spinal cord and brain atrophy are common in neuromyelitis optica spectrum disorder (NMOSD) and relapsing-remitting multiple sclerosis (RRMS) but harbor distinct patterns accounting for disability and cognitive impairment.
Methods
This study included 209 NMOSD and 304 RRMS patients and 436 healthy controls. Non-negative matrix factorization was used to parse differences in spinal cord and brain atrophy at subject level into distinct patterns based on structural MRI. The weights of patterns were obtained using a linear regression model and associated with Expanded Disability Status Scale (EDSS) and cognitive scores. Additionally, patients were divided into cognitive impairment (CI) and cognitive preservation (CP) groups.
Results
Three patterns were observed in NMOSD: (1) Spinal Cord-Deep Grey Matter (SC-DGM) pattern was associated with high EDSS scores and decline of visuospatial memory function; (2) Frontal-Temporal pattern was associated with decline of language learning function; and (3) Cerebellum-Brainstem pattern had no observed association. Patients with CI had higher weights of SC-DGM pattern than CP group. Three patterns were observed in RRMS: (1) DGM pattern was associated with high EDSS scores, decreased information processing speed, and decreased language learning and visuospatial memory functions; (2) Frontal-Temporal pattern was associated with overall cognitive decline; and (3) Occipital pattern had no observed association. Patients with CI trended to have higher weights of DGM and Frontal-Temporal patterns than CP group.
Conclusion
This study estimated the heterogeneity of spinal cord and brain atrophy patterns in NMOSD and RRMS patients at individual level, and evaluated the clinical relevance of these patterns, which may contribute to stratifying participants for targeted therapy.</description><subject>Adult</subject><subject>Atrophy</subject><subject>Atrophy - pathology</subject><subject>Brain - diagnostic imaging</subject><subject>Brain - pathology</subject><subject>Brain stem</subject><subject>Cerebellum</subject><subject>Cognitive ability</subject><subject>Cognitive Dysfunction - diagnostic imaging</subject><subject>Cognitive Dysfunction - etiology</subject><subject>Cognitive Dysfunction - pathology</subject><subject>Cognitive Dysfunction - physiopathology</subject><subject>Female</subject><subject>Gray Matter - diagnostic imaging</subject><subject>Gray Matter - pathology</subject><subject>Humans</subject><subject>Information processing</subject><subject>Learning</subject><subject>Magnetic Resonance Imaging</subject><subject>Male</subject><subject>Medicine</subject><subject>Medicine & Public Health</subject><subject>Memory</subject><subject>Middle Aged</subject><subject>Multiple sclerosis</subject><subject>Multiple Sclerosis, Relapsing-Remitting - diagnostic imaging</subject><subject>Multiple Sclerosis, Relapsing-Remitting - pathology</subject><subject>Multiple Sclerosis, Relapsing-Remitting - physiopathology</subject><subject>Neurology</subject><subject>Neuromyelitis</subject><subject>Neuromyelitis Optica - diagnostic imaging</subject><subject>Neuromyelitis Optica - pathology</subject><subject>Neuroradiology</subject><subject>Neurosciences</subject><subject>Original Communication</subject><subject>Spatial memory</subject><subject>Spinal cord</subject><subject>Spinal Cord - diagnostic imaging</subject><subject>Spinal Cord - pathology</subject><subject>Substantia grisea</subject><issn>0340-5354</issn><issn>1432-1459</issn><issn>1432-1459</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kclKBDEQhoMoOi4v4EECXry0VtZJH0XcQPCgnkM6nR4z9GaSPszbm5lxAQ-eAqmvvqLqR-iUwCUBmF9FAE5EAZQXhFJFinIHzQhntCBclLtoBoxDIZjgB-gwxiUAqFzYRwdMCaEIL2do8TL63rTYDqHGpq9xFYzvsUlhGN9XeDQpudBHnP96N4WhW7nWJx_xMCZvDY6jsylMHa59zAoXNpJuapMfW4ejbV0Yoo_HaK8xbXQnX-8Reru7fb15KJ6e7x9vrp8Ky6hMxZzXphKlFM4AA1spxUthVCnnzFYNV7KqGyuZAakErxrblE0DQhoqJBW0luwIXWy9Yxg-JheT7ny0rm1N74YpagaMkDyKr9HzP-hymEI-xpqSRAAHoTJFt5TNe8TgGj0G35mw0gT0Oga9jUHnGPQmBl3mprMv9VR1rv5p-b57BtgWiLnUL1z4nf2P9hPYgpPd</recordid><startdate>20240601</startdate><enddate>20240601</enddate><creator>Hua, Tiantian</creator><creator>Fan, Houyou</creator><creator>Duan, Yunyun</creator><creator>Tian, Decai</creator><creator>Chen, Zhenpeng</creator><creator>Xu, Xiaolu</creator><creator>Bai, Yutong</creator><creator>Li, Yuna</creator><creator>Zhang, Ningnannan</creator><creator>Sun, Jie</creator><creator>Li, Haiqing</creator><creator>Li, Yuxin</creator><creator>Li, Yongmei</creator><creator>Zeng, Chun</creator><creator>Han, Xuemei</creator><creator>Zhou, Fuqing</creator><creator>Huang, Muhua</creator><creator>Xu, Siyao</creator><creator>Jin, Ying</creator><creator>Li, Hongfang</creator><creator>Zhuo, Zhizheng</creator><creator>Zhang, Xinghu</creator><creator>Liu, Yaou</creator><general>Springer Berlin Heidelberg</general><general>Springer Nature B.V</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>7TK</scope><scope>K9.</scope><scope>7X8</scope></search><sort><creationdate>20240601</creationdate><title>Spinal cord and brain atrophy patterns in neuromyelitis optica spectrum disorder and multiple sclerosis</title><author>Hua, Tiantian ; Fan, Houyou ; Duan, Yunyun ; Tian, Decai ; Chen, Zhenpeng ; Xu, Xiaolu ; Bai, Yutong ; Li, Yuna ; Zhang, Ningnannan ; Sun, Jie ; Li, Haiqing ; Li, Yuxin ; Li, Yongmei ; Zeng, Chun ; Han, Xuemei ; Zhou, Fuqing ; Huang, Muhua ; Xu, Siyao ; Jin, Ying ; Li, Hongfang ; Zhuo, Zhizheng ; Zhang, Xinghu ; Liu, Yaou</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c326t-74dab5965ea030cb88495a89673cbf486bdfc63a06854bfcf9ff056a256252d63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Adult</topic><topic>Atrophy</topic><topic>Atrophy - pathology</topic><topic>Brain - diagnostic imaging</topic><topic>Brain - pathology</topic><topic>Brain stem</topic><topic>Cerebellum</topic><topic>Cognitive ability</topic><topic>Cognitive Dysfunction - diagnostic imaging</topic><topic>Cognitive Dysfunction - etiology</topic><topic>Cognitive Dysfunction - pathology</topic><topic>Cognitive Dysfunction - physiopathology</topic><topic>Female</topic><topic>Gray Matter - diagnostic imaging</topic><topic>Gray Matter - pathology</topic><topic>Humans</topic><topic>Information processing</topic><topic>Learning</topic><topic>Magnetic Resonance Imaging</topic><topic>Male</topic><topic>Medicine</topic><topic>Medicine & Public Health</topic><topic>Memory</topic><topic>Middle Aged</topic><topic>Multiple sclerosis</topic><topic>Multiple Sclerosis, Relapsing-Remitting - diagnostic imaging</topic><topic>Multiple Sclerosis, Relapsing-Remitting - pathology</topic><topic>Multiple Sclerosis, Relapsing-Remitting - physiopathology</topic><topic>Neurology</topic><topic>Neuromyelitis</topic><topic>Neuromyelitis Optica - diagnostic imaging</topic><topic>Neuromyelitis Optica - pathology</topic><topic>Neuroradiology</topic><topic>Neurosciences</topic><topic>Original Communication</topic><topic>Spatial memory</topic><topic>Spinal cord</topic><topic>Spinal Cord - diagnostic imaging</topic><topic>Spinal Cord - pathology</topic><topic>Substantia grisea</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hua, Tiantian</creatorcontrib><creatorcontrib>Fan, Houyou</creatorcontrib><creatorcontrib>Duan, Yunyun</creatorcontrib><creatorcontrib>Tian, Decai</creatorcontrib><creatorcontrib>Chen, Zhenpeng</creatorcontrib><creatorcontrib>Xu, Xiaolu</creatorcontrib><creatorcontrib>Bai, Yutong</creatorcontrib><creatorcontrib>Li, Yuna</creatorcontrib><creatorcontrib>Zhang, Ningnannan</creatorcontrib><creatorcontrib>Sun, Jie</creatorcontrib><creatorcontrib>Li, Haiqing</creatorcontrib><creatorcontrib>Li, Yuxin</creatorcontrib><creatorcontrib>Li, Yongmei</creatorcontrib><creatorcontrib>Zeng, Chun</creatorcontrib><creatorcontrib>Han, Xuemei</creatorcontrib><creatorcontrib>Zhou, Fuqing</creatorcontrib><creatorcontrib>Huang, Muhua</creatorcontrib><creatorcontrib>Xu, Siyao</creatorcontrib><creatorcontrib>Jin, Ying</creatorcontrib><creatorcontrib>Li, Hongfang</creatorcontrib><creatorcontrib>Zhuo, Zhizheng</creatorcontrib><creatorcontrib>Zhang, Xinghu</creatorcontrib><creatorcontrib>Liu, Yaou</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><jtitle>Journal of neurology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hua, Tiantian</au><au>Fan, Houyou</au><au>Duan, Yunyun</au><au>Tian, Decai</au><au>Chen, Zhenpeng</au><au>Xu, Xiaolu</au><au>Bai, Yutong</au><au>Li, Yuna</au><au>Zhang, Ningnannan</au><au>Sun, Jie</au><au>Li, Haiqing</au><au>Li, Yuxin</au><au>Li, Yongmei</au><au>Zeng, Chun</au><au>Han, Xuemei</au><au>Zhou, Fuqing</au><au>Huang, Muhua</au><au>Xu, Siyao</au><au>Jin, Ying</au><au>Li, Hongfang</au><au>Zhuo, Zhizheng</au><au>Zhang, Xinghu</au><au>Liu, Yaou</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Spinal cord and brain atrophy patterns in neuromyelitis optica spectrum disorder and multiple sclerosis</atitle><jtitle>Journal of neurology</jtitle><stitle>J Neurol</stitle><addtitle>J Neurol</addtitle><date>2024-06-01</date><risdate>2024</risdate><volume>271</volume><issue>6</issue><spage>3595</spage><epage>3609</epage><pages>3595-3609</pages><issn>0340-5354</issn><issn>1432-1459</issn><eissn>1432-1459</eissn><abstract>Background
Spinal cord and brain atrophy are common in neuromyelitis optica spectrum disorder (NMOSD) and relapsing-remitting multiple sclerosis (RRMS) but harbor distinct patterns accounting for disability and cognitive impairment.
Methods
This study included 209 NMOSD and 304 RRMS patients and 436 healthy controls. Non-negative matrix factorization was used to parse differences in spinal cord and brain atrophy at subject level into distinct patterns based on structural MRI. The weights of patterns were obtained using a linear regression model and associated with Expanded Disability Status Scale (EDSS) and cognitive scores. Additionally, patients were divided into cognitive impairment (CI) and cognitive preservation (CP) groups.
Results
Three patterns were observed in NMOSD: (1) Spinal Cord-Deep Grey Matter (SC-DGM) pattern was associated with high EDSS scores and decline of visuospatial memory function; (2) Frontal-Temporal pattern was associated with decline of language learning function; and (3) Cerebellum-Brainstem pattern had no observed association. Patients with CI had higher weights of SC-DGM pattern than CP group. Three patterns were observed in RRMS: (1) DGM pattern was associated with high EDSS scores, decreased information processing speed, and decreased language learning and visuospatial memory functions; (2) Frontal-Temporal pattern was associated with overall cognitive decline; and (3) Occipital pattern had no observed association. Patients with CI trended to have higher weights of DGM and Frontal-Temporal patterns than CP group.
Conclusion
This study estimated the heterogeneity of spinal cord and brain atrophy patterns in NMOSD and RRMS patients at individual level, and evaluated the clinical relevance of these patterns, which may contribute to stratifying participants for targeted therapy.</abstract><cop>Berlin/Heidelberg</cop><pub>Springer Berlin Heidelberg</pub><pmid>38558149</pmid><doi>10.1007/s00415-024-12281-9</doi><tpages>15</tpages></addata></record> |
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subjects | Adult Atrophy Atrophy - pathology Brain - diagnostic imaging Brain - pathology Brain stem Cerebellum Cognitive ability Cognitive Dysfunction - diagnostic imaging Cognitive Dysfunction - etiology Cognitive Dysfunction - pathology Cognitive Dysfunction - physiopathology Female Gray Matter - diagnostic imaging Gray Matter - pathology Humans Information processing Learning Magnetic Resonance Imaging Male Medicine Medicine & Public Health Memory Middle Aged Multiple sclerosis Multiple Sclerosis, Relapsing-Remitting - diagnostic imaging Multiple Sclerosis, Relapsing-Remitting - pathology Multiple Sclerosis, Relapsing-Remitting - physiopathology Neurology Neuromyelitis Neuromyelitis Optica - diagnostic imaging Neuromyelitis Optica - pathology Neuroradiology Neurosciences Original Communication Spatial memory Spinal cord Spinal Cord - diagnostic imaging Spinal Cord - pathology Substantia grisea |
title | Spinal cord and brain atrophy patterns in neuromyelitis optica spectrum disorder and multiple sclerosis |
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