Fiber‐specific white matter analysis reflects upper motor neuron impairment in amyotrophic lateral sclerosis
Background and purpose To clarify the relationship between fiber‐specific white matter changes in amyotrophic lateral sclerosis (ALS) and clinical signs of upper motor neuron (UMN) involvement, we performed a fixel‐based analysis (FBA), a novel framework for diffusion‐weighted imaging analysis. Meth...
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| Veröffentlicht in: | European journal of neurology 2022-02, Vol.29 (2), p.432-440 |
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| creator | Ogura, Aya Kawabata, Kazuya Watanabe, Hirohisa Choy, Shao Wei Bagarinao, Epifanio Kato, Toshiyasu Imai, Kazunori Masuda, Michihito Ohdake, Reiko Hara, Kazuhiro Nakamura, Ryoichi Atsuta, Naoki Nakamura, Tomohiko Katsuno, Masahisa Sobue, Gen |
| description | Background and purpose
To clarify the relationship between fiber‐specific white matter changes in amyotrophic lateral sclerosis (ALS) and clinical signs of upper motor neuron (UMN) involvement, we performed a fixel‐based analysis (FBA), a novel framework for diffusion‐weighted imaging analysis.
Methods
We enrolled 96 participants, including 48 nonfamilial ALS patients and 48 age‐ and sex‐matched healthy controls (HCs), in this study and conducted whole‐brain FBA and voxel‐based morphometry analysis. We compared the fiber density (FD), fiber morphology (fiber cross‐section [FC]), and a combined index of FD and FC (FDC) between the ALS and HC groups. We performed a tract‐of‐interest analysis to extract FD values across the significant regions in the whole‐brain analysis. Then, we evaluated the associations between FD values and clinical variables.
Results
The bilateral corticospinal tracts (CSTs) and the corpus callosum (CC) showed reduced FD and FDC in ALS patients compared with HCs (p |
| doi_str_mv | 10.1111/ene.15136 |
| format | Article |
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To clarify the relationship between fiber‐specific white matter changes in amyotrophic lateral sclerosis (ALS) and clinical signs of upper motor neuron (UMN) involvement, we performed a fixel‐based analysis (FBA), a novel framework for diffusion‐weighted imaging analysis.
Methods
We enrolled 96 participants, including 48 nonfamilial ALS patients and 48 age‐ and sex‐matched healthy controls (HCs), in this study and conducted whole‐brain FBA and voxel‐based morphometry analysis. We compared the fiber density (FD), fiber morphology (fiber cross‐section [FC]), and a combined index of FD and FC (FDC) between the ALS and HC groups. We performed a tract‐of‐interest analysis to extract FD values across the significant regions in the whole‐brain analysis. Then, we evaluated the associations between FD values and clinical variables.
Results
The bilateral corticospinal tracts (CSTs) and the corpus callosum (CC) showed reduced FD and FDC in ALS patients compared with HCs (p < 0.05, familywise error‐corrected), and the comparison of FCs revealed no region that was significantly different from another. Voxel‐based morphometry showed cortical volume reduction in the regions, including the primary motor area. Clinical scores showed correlations with FD values in the CSTs (UMN score: rho = −0.530, p < 0.001; central motor conduction time [CMCT] in the upper limb: rho = −0.474, p = 0.008; disease duration: rho = −0.383, p = 0.007; ALS Functional Rating Scale‐Revised: rho = 0.340, p = 0.018). In addition, patients whose CMCT was not calculated due to unevoked waves also showed FD reduction in the CSTs.
Conclusions
Our findings suggest that FD values in the CST estimated via FBA can be potentially used in evaluating UMN impairments.
Fixel‐based analysis revealed reduced fiber density (FD) in the corticospinal tracts (CSTs) in amyotrophic lateral sclerosis patients. The FD reduction in the CSTs and upper motor neuron (UMN) impairments were correlated. We report that FD values in the CST estimated via FBA can be potentially used in evaluating UMN impairments.</description><identifier>ISSN: 1351-5101</identifier><identifier>EISSN: 1468-1331</identifier><identifier>DOI: 10.1111/ene.15136</identifier><identifier>PMID: 34632672</identifier><language>eng</language><publisher>England: John Wiley & Sons, Inc</publisher><subject>Amyotrophic lateral sclerosis ; Brain ; Corpus callosum ; corticospinal tract ; diffusion‐weighted imaging ; Error correction ; fixel‐based analysis ; Morphometry ; Neuroimaging ; Patients ; Pyramidal tracts ; Reduction ; Substantia alba ; upper motor neuron signs</subject><ispartof>European journal of neurology, 2022-02, Vol.29 (2), p.432-440</ispartof><rights>2021 European Academy of Neurology</rights><rights>2021 European Academy of Neurology.</rights><rights>Copyright © 2022 European Academy of Neurology</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4196-d4b522fb35172965d1c2ca45a1fd751b39c2066a755fe7d8e9a41e6441b384e13</citedby><cites>FETCH-LOGICAL-c4196-d4b522fb35172965d1c2ca45a1fd751b39c2066a755fe7d8e9a41e6441b384e13</cites><orcidid>0000-0001-8553-8536 ; 0000-0001-5000-6943 ; 0000-0002-8851-4377 ; 0000-0003-0928-8605 ; 0000-0003-4769-5922 ; 0000-0001-7622-4527 ; 0000-0001-9453-9311</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fene.15136$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fene.15136$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34632672$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ogura, Aya</creatorcontrib><creatorcontrib>Kawabata, Kazuya</creatorcontrib><creatorcontrib>Watanabe, Hirohisa</creatorcontrib><creatorcontrib>Choy, Shao Wei</creatorcontrib><creatorcontrib>Bagarinao, Epifanio</creatorcontrib><creatorcontrib>Kato, Toshiyasu</creatorcontrib><creatorcontrib>Imai, Kazunori</creatorcontrib><creatorcontrib>Masuda, Michihito</creatorcontrib><creatorcontrib>Ohdake, Reiko</creatorcontrib><creatorcontrib>Hara, Kazuhiro</creatorcontrib><creatorcontrib>Nakamura, Ryoichi</creatorcontrib><creatorcontrib>Atsuta, Naoki</creatorcontrib><creatorcontrib>Nakamura, Tomohiko</creatorcontrib><creatorcontrib>Katsuno, Masahisa</creatorcontrib><creatorcontrib>Sobue, Gen</creatorcontrib><title>Fiber‐specific white matter analysis reflects upper motor neuron impairment in amyotrophic lateral sclerosis</title><title>European journal of neurology</title><addtitle>Eur J Neurol</addtitle><description>Background and purpose
To clarify the relationship between fiber‐specific white matter changes in amyotrophic lateral sclerosis (ALS) and clinical signs of upper motor neuron (UMN) involvement, we performed a fixel‐based analysis (FBA), a novel framework for diffusion‐weighted imaging analysis.
Methods
We enrolled 96 participants, including 48 nonfamilial ALS patients and 48 age‐ and sex‐matched healthy controls (HCs), in this study and conducted whole‐brain FBA and voxel‐based morphometry analysis. We compared the fiber density (FD), fiber morphology (fiber cross‐section [FC]), and a combined index of FD and FC (FDC) between the ALS and HC groups. We performed a tract‐of‐interest analysis to extract FD values across the significant regions in the whole‐brain analysis. Then, we evaluated the associations between FD values and clinical variables.
Results
The bilateral corticospinal tracts (CSTs) and the corpus callosum (CC) showed reduced FD and FDC in ALS patients compared with HCs (p < 0.05, familywise error‐corrected), and the comparison of FCs revealed no region that was significantly different from another. Voxel‐based morphometry showed cortical volume reduction in the regions, including the primary motor area. Clinical scores showed correlations with FD values in the CSTs (UMN score: rho = −0.530, p < 0.001; central motor conduction time [CMCT] in the upper limb: rho = −0.474, p = 0.008; disease duration: rho = −0.383, p = 0.007; ALS Functional Rating Scale‐Revised: rho = 0.340, p = 0.018). In addition, patients whose CMCT was not calculated due to unevoked waves also showed FD reduction in the CSTs.
Conclusions
Our findings suggest that FD values in the CST estimated via FBA can be potentially used in evaluating UMN impairments.
Fixel‐based analysis revealed reduced fiber density (FD) in the corticospinal tracts (CSTs) in amyotrophic lateral sclerosis patients. The FD reduction in the CSTs and upper motor neuron (UMN) impairments were correlated. We report that FD values in the CST estimated via FBA can be potentially used in evaluating UMN impairments.</description><subject>Amyotrophic lateral sclerosis</subject><subject>Brain</subject><subject>Corpus callosum</subject><subject>corticospinal tract</subject><subject>diffusion‐weighted imaging</subject><subject>Error correction</subject><subject>fixel‐based analysis</subject><subject>Morphometry</subject><subject>Neuroimaging</subject><subject>Patients</subject><subject>Pyramidal tracts</subject><subject>Reduction</subject><subject>Substantia alba</subject><subject>upper motor neuron signs</subject><issn>1351-5101</issn><issn>1468-1331</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><recordid>eNp1kc1O3TAQRi1UVH7aRV-gstQNLAIex3aSZYUutBKiG7qOHGcijJw4tROhu-MR-ow8CVMudFGp3tgaHx3NzMfYJxBnQOccJzwDDaXZY4egTF1AWcI7epcaCg0CDthRzvdCCFlJ8Z4dlMqU0lTykE2XvsP09Pg7z-j84B1_uPML8tEuCyZuJxu22WeecAjolszXeab6GJeY-IRrihP342x9GnFauJ-4HbdxSXG-I1ewJLGBZxcwRfJ8YPuDDRk_vt7H7Ofl5vbiW3H94-r7xdfrwiloTNGrTks5dNR_JRuje3DSWaUtDH2loSsbJ4UxttJ6wKqvsbEK0ChFX7VCKI_Zyc47p_hrxby0o88OQ7ATxjW3UteiUULrhtAv_6D3cU00N1EG6qrWFdREne4oR3Nk2kY7Jz_atG1BtH9CaCmE9iUEYj-_GtduxP4v-bZ1As53wIMPuP2_qd3cbHbKZ8UkkpI</recordid><startdate>202202</startdate><enddate>202202</enddate><creator>Ogura, Aya</creator><creator>Kawabata, Kazuya</creator><creator>Watanabe, Hirohisa</creator><creator>Choy, Shao Wei</creator><creator>Bagarinao, Epifanio</creator><creator>Kato, Toshiyasu</creator><creator>Imai, Kazunori</creator><creator>Masuda, Michihito</creator><creator>Ohdake, Reiko</creator><creator>Hara, Kazuhiro</creator><creator>Nakamura, Ryoichi</creator><creator>Atsuta, Naoki</creator><creator>Nakamura, Tomohiko</creator><creator>Katsuno, Masahisa</creator><creator>Sobue, Gen</creator><general>John Wiley & Sons, Inc</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7TK</scope><scope>7U7</scope><scope>C1K</scope><scope>K9.</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-8553-8536</orcidid><orcidid>https://orcid.org/0000-0001-5000-6943</orcidid><orcidid>https://orcid.org/0000-0002-8851-4377</orcidid><orcidid>https://orcid.org/0000-0003-0928-8605</orcidid><orcidid>https://orcid.org/0000-0003-4769-5922</orcidid><orcidid>https://orcid.org/0000-0001-7622-4527</orcidid><orcidid>https://orcid.org/0000-0001-9453-9311</orcidid></search><sort><creationdate>202202</creationdate><title>Fiber‐specific white matter analysis reflects upper motor neuron impairment in amyotrophic lateral sclerosis</title><author>Ogura, Aya ; Kawabata, Kazuya ; Watanabe, Hirohisa ; Choy, Shao Wei ; Bagarinao, Epifanio ; Kato, Toshiyasu ; Imai, Kazunori ; Masuda, Michihito ; Ohdake, Reiko ; Hara, Kazuhiro ; Nakamura, Ryoichi ; Atsuta, Naoki ; Nakamura, Tomohiko ; Katsuno, Masahisa ; Sobue, Gen</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4196-d4b522fb35172965d1c2ca45a1fd751b39c2066a755fe7d8e9a41e6441b384e13</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Amyotrophic lateral sclerosis</topic><topic>Brain</topic><topic>Corpus callosum</topic><topic>corticospinal tract</topic><topic>diffusion‐weighted imaging</topic><topic>Error correction</topic><topic>fixel‐based analysis</topic><topic>Morphometry</topic><topic>Neuroimaging</topic><topic>Patients</topic><topic>Pyramidal tracts</topic><topic>Reduction</topic><topic>Substantia alba</topic><topic>upper motor neuron signs</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ogura, Aya</creatorcontrib><creatorcontrib>Kawabata, Kazuya</creatorcontrib><creatorcontrib>Watanabe, Hirohisa</creatorcontrib><creatorcontrib>Choy, Shao Wei</creatorcontrib><creatorcontrib>Bagarinao, Epifanio</creatorcontrib><creatorcontrib>Kato, Toshiyasu</creatorcontrib><creatorcontrib>Imai, Kazunori</creatorcontrib><creatorcontrib>Masuda, Michihito</creatorcontrib><creatorcontrib>Ohdake, Reiko</creatorcontrib><creatorcontrib>Hara, Kazuhiro</creatorcontrib><creatorcontrib>Nakamura, Ryoichi</creatorcontrib><creatorcontrib>Atsuta, Naoki</creatorcontrib><creatorcontrib>Nakamura, Tomohiko</creatorcontrib><creatorcontrib>Katsuno, Masahisa</creatorcontrib><creatorcontrib>Sobue, Gen</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><jtitle>European journal of neurology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ogura, Aya</au><au>Kawabata, Kazuya</au><au>Watanabe, Hirohisa</au><au>Choy, Shao Wei</au><au>Bagarinao, Epifanio</au><au>Kato, Toshiyasu</au><au>Imai, Kazunori</au><au>Masuda, Michihito</au><au>Ohdake, Reiko</au><au>Hara, Kazuhiro</au><au>Nakamura, Ryoichi</au><au>Atsuta, Naoki</au><au>Nakamura, Tomohiko</au><au>Katsuno, Masahisa</au><au>Sobue, Gen</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Fiber‐specific white matter analysis reflects upper motor neuron impairment in amyotrophic lateral sclerosis</atitle><jtitle>European journal of neurology</jtitle><addtitle>Eur J Neurol</addtitle><date>2022-02</date><risdate>2022</risdate><volume>29</volume><issue>2</issue><spage>432</spage><epage>440</epage><pages>432-440</pages><issn>1351-5101</issn><eissn>1468-1331</eissn><abstract>Background and purpose
To clarify the relationship between fiber‐specific white matter changes in amyotrophic lateral sclerosis (ALS) and clinical signs of upper motor neuron (UMN) involvement, we performed a fixel‐based analysis (FBA), a novel framework for diffusion‐weighted imaging analysis.
Methods
We enrolled 96 participants, including 48 nonfamilial ALS patients and 48 age‐ and sex‐matched healthy controls (HCs), in this study and conducted whole‐brain FBA and voxel‐based morphometry analysis. We compared the fiber density (FD), fiber morphology (fiber cross‐section [FC]), and a combined index of FD and FC (FDC) between the ALS and HC groups. We performed a tract‐of‐interest analysis to extract FD values across the significant regions in the whole‐brain analysis. Then, we evaluated the associations between FD values and clinical variables.
Results
The bilateral corticospinal tracts (CSTs) and the corpus callosum (CC) showed reduced FD and FDC in ALS patients compared with HCs (p < 0.05, familywise error‐corrected), and the comparison of FCs revealed no region that was significantly different from another. Voxel‐based morphometry showed cortical volume reduction in the regions, including the primary motor area. Clinical scores showed correlations with FD values in the CSTs (UMN score: rho = −0.530, p < 0.001; central motor conduction time [CMCT] in the upper limb: rho = −0.474, p = 0.008; disease duration: rho = −0.383, p = 0.007; ALS Functional Rating Scale‐Revised: rho = 0.340, p = 0.018). In addition, patients whose CMCT was not calculated due to unevoked waves also showed FD reduction in the CSTs.
Conclusions
Our findings suggest that FD values in the CST estimated via FBA can be potentially used in evaluating UMN impairments.
Fixel‐based analysis revealed reduced fiber density (FD) in the corticospinal tracts (CSTs) in amyotrophic lateral sclerosis patients. The FD reduction in the CSTs and upper motor neuron (UMN) impairments were correlated. We report that FD values in the CST estimated via FBA can be potentially used in evaluating UMN impairments.</abstract><cop>England</cop><pub>John Wiley & Sons, Inc</pub><pmid>34632672</pmid><doi>10.1111/ene.15136</doi><tpages>9</tpages><orcidid>https://orcid.org/0000-0001-8553-8536</orcidid><orcidid>https://orcid.org/0000-0001-5000-6943</orcidid><orcidid>https://orcid.org/0000-0002-8851-4377</orcidid><orcidid>https://orcid.org/0000-0003-0928-8605</orcidid><orcidid>https://orcid.org/0000-0003-4769-5922</orcidid><orcidid>https://orcid.org/0000-0001-7622-4527</orcidid><orcidid>https://orcid.org/0000-0001-9453-9311</orcidid></addata></record> |
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| source | Wiley Online Library Journals Frontfile Complete |
| subjects | Amyotrophic lateral sclerosis Brain Corpus callosum corticospinal tract diffusion‐weighted imaging Error correction fixel‐based analysis Morphometry Neuroimaging Patients Pyramidal tracts Reduction Substantia alba upper motor neuron signs |
| title | Fiber‐specific white matter analysis reflects upper motor neuron impairment in amyotrophic lateral sclerosis |
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