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
Hauptverfasser: 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
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container_end_page 3609
container_issue 6
container_start_page 3595
container_title Journal of neurology
container_volume 271
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
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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 &amp; 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 &amp; 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 &amp; 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 &amp; 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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