Fixel-Based Analysis Reveals Tau-Related White Matter Changes in Early Stages of Alzheimer's Disease
Several studies have shown white matter (WM) abnormalities in Alzheimer's disease (AD) using diffusion tensor imaging (DTI). Nonetheless, robust characterization of WM changes has been challenging due to the methodological limitations of DTI. We applied fixel-based analyses (FBA) to examine mic...
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| Veröffentlicht in: | The Journal of neuroscience 2024-05, Vol.44 (18), p.e0538232024 |
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| creator | Ahmadi, Khazar Pereira, Joana B van Westen, Danielle Pasternak, Ofer Zhang, Fan Nilsson, Markus Stomrud, Erik Spotorno, Nicola Hansson, Oskar |
| description | Several studies have shown white matter (WM) abnormalities in Alzheimer's disease (AD) using diffusion tensor imaging (DTI). Nonetheless, robust characterization of WM changes has been challenging due to the methodological limitations of DTI. We applied fixel-based analyses (FBA) to examine microscopic differences in fiber density (FD) and macroscopic changes in fiber cross-section (FC) in early stages of AD (
= 393, 212 females). FBA was also compared with DTI, free-water corrected (FW)-DTI and diffusion kurtosis imaging (DKI). We further investigated the correlation of FBA and tensor-derived metrics with AD pathology and cognition. FBA metrics were decreased in the entire cingulum bundle, uncinate fasciculus and anterior thalamic radiations in Aβ-positive patients with mild cognitive impairment compared to control groups. Metrics derived from DKI, and FW-DTI showed similar alterations whereas WM degeneration detected by DTI was more widespread. Tau-PET uptake in medial temporal regions was only correlated with reduced FC mainly in the parahippocampal cingulum in Aβ-positive individuals. This tau-related WM alteration was also associated with impaired memory. Despite the spatially extensive between-group differences in DTI-metrics, the link between WM and tau aggregation was only revealed using FBA metrics implying high sensitivity but low specificity of DTI-based measures in identifying subtle tau-related WM degeneration. No relationship was found between amyloid load and any diffusion-MRI measures. Our results indicate that early tau-related WM alterations in AD are due to macrostructural changes specifically captured by FBA metrics. Thus, future studies assessing the effects of AD pathology in WM tracts should consider using FBA metrics. |
| doi_str_mv | 10.1523/JNEUROSCI.0538-23.2024 |
| format | Article |
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= 393, 212 females). FBA was also compared with DTI, free-water corrected (FW)-DTI and diffusion kurtosis imaging (DKI). We further investigated the correlation of FBA and tensor-derived metrics with AD pathology and cognition. FBA metrics were decreased in the entire cingulum bundle, uncinate fasciculus and anterior thalamic radiations in Aβ-positive patients with mild cognitive impairment compared to control groups. Metrics derived from DKI, and FW-DTI showed similar alterations whereas WM degeneration detected by DTI was more widespread. Tau-PET uptake in medial temporal regions was only correlated with reduced FC mainly in the parahippocampal cingulum in Aβ-positive individuals. This tau-related WM alteration was also associated with impaired memory. Despite the spatially extensive between-group differences in DTI-metrics, the link between WM and tau aggregation was only revealed using FBA metrics implying high sensitivity but low specificity of DTI-based measures in identifying subtle tau-related WM degeneration. No relationship was found between amyloid load and any diffusion-MRI measures. Our results indicate that early tau-related WM alterations in AD are due to macrostructural changes specifically captured by FBA metrics. Thus, future studies assessing the effects of AD pathology in WM tracts should consider using FBA metrics.</description><identifier>ISSN: 0270-6474</identifier><identifier>EISSN: 1529-2401</identifier><identifier>DOI: 10.1523/JNEUROSCI.0538-23.2024</identifier><identifier>PMID: 38565289</identifier><language>eng</language><publisher>United States: Society for Neuroscience</publisher><subject>Abnormalities ; Aged ; Aged, 80 and over ; Aggregation ; Alzheimer Disease - diagnostic imaging ; Alzheimer Disease - metabolism ; Alzheimer Disease - pathology ; Alzheimer's disease ; Cingulum ; Clinical Medicine ; Cognition ; Cognitive ability ; Cognitive Dysfunction - diagnostic imaging ; Cognitive Dysfunction - pathology ; Degeneration ; Diffusion ; diffusion tensor imaging ; Diffusion Tensor Imaging - methods ; Female ; fixel-based analysis ; Humans ; Klinisk medicin ; Kurtosis ; Magnetic resonance imaging ; Male ; Medical and Health Sciences ; Medical imaging ; Medicin och hälsovetenskap ; memory ; Middle Aged ; Neurodegenerative diseases ; Pathology ; Positron emission ; Radiologi och bildbehandling ; Radiology, Nuclear Medicine and Medical Imaging ; Substantia alba ; Tau protein ; tau Proteins - metabolism ; Tensors ; Thalamus ; white matter ; White Matter - diagnostic imaging ; White Matter - pathology ; β-Amyloid</subject><ispartof>The Journal of neuroscience, 2024-05, Vol.44 (18), p.e0538232024</ispartof><rights>Copyright © 2024 Ahmadi et al.</rights><rights>Copyright Society for Neuroscience May 1, 2024</rights><rights>Copyright © 2024 Ahmadi et al. 2024</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><orcidid>0000-0002-3371-6211</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11063818/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11063818/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,550,723,776,780,881,27903,27904,53769,53771</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38565289$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://lup.lub.lu.se/record/9ee57644-6711-4f22-baf1-59bd4d4f079a$$DView record from Swedish Publication Index$$Hfree_for_read</backlink><backlink>$$Uhttp://kipublications.ki.se/Default.aspx?queryparsed=id:158532578$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><creatorcontrib>Ahmadi, Khazar</creatorcontrib><creatorcontrib>Pereira, Joana B</creatorcontrib><creatorcontrib>van Westen, Danielle</creatorcontrib><creatorcontrib>Pasternak, Ofer</creatorcontrib><creatorcontrib>Zhang, Fan</creatorcontrib><creatorcontrib>Nilsson, Markus</creatorcontrib><creatorcontrib>Stomrud, Erik</creatorcontrib><creatorcontrib>Spotorno, Nicola</creatorcontrib><creatorcontrib>Hansson, Oskar</creatorcontrib><title>Fixel-Based Analysis Reveals Tau-Related White Matter Changes in Early Stages of Alzheimer's Disease</title><title>The Journal of neuroscience</title><addtitle>J Neurosci</addtitle><description>Several studies have shown white matter (WM) abnormalities in Alzheimer's disease (AD) using diffusion tensor imaging (DTI). Nonetheless, robust characterization of WM changes has been challenging due to the methodological limitations of DTI. We applied fixel-based analyses (FBA) to examine microscopic differences in fiber density (FD) and macroscopic changes in fiber cross-section (FC) in early stages of AD (
= 393, 212 females). FBA was also compared with DTI, free-water corrected (FW)-DTI and diffusion kurtosis imaging (DKI). We further investigated the correlation of FBA and tensor-derived metrics with AD pathology and cognition. FBA metrics were decreased in the entire cingulum bundle, uncinate fasciculus and anterior thalamic radiations in Aβ-positive patients with mild cognitive impairment compared to control groups. Metrics derived from DKI, and FW-DTI showed similar alterations whereas WM degeneration detected by DTI was more widespread. Tau-PET uptake in medial temporal regions was only correlated with reduced FC mainly in the parahippocampal cingulum in Aβ-positive individuals. This tau-related WM alteration was also associated with impaired memory. Despite the spatially extensive between-group differences in DTI-metrics, the link between WM and tau aggregation was only revealed using FBA metrics implying high sensitivity but low specificity of DTI-based measures in identifying subtle tau-related WM degeneration. No relationship was found between amyloid load and any diffusion-MRI measures. Our results indicate that early tau-related WM alterations in AD are due to macrostructural changes specifically captured by FBA metrics. Thus, future studies assessing the effects of AD pathology in WM tracts should consider using FBA metrics.</description><subject>Abnormalities</subject><subject>Aged</subject><subject>Aged, 80 and over</subject><subject>Aggregation</subject><subject>Alzheimer Disease - diagnostic imaging</subject><subject>Alzheimer Disease - metabolism</subject><subject>Alzheimer Disease - pathology</subject><subject>Alzheimer's disease</subject><subject>Cingulum</subject><subject>Clinical Medicine</subject><subject>Cognition</subject><subject>Cognitive ability</subject><subject>Cognitive Dysfunction - diagnostic imaging</subject><subject>Cognitive Dysfunction - pathology</subject><subject>Degeneration</subject><subject>Diffusion</subject><subject>diffusion tensor imaging</subject><subject>Diffusion Tensor Imaging - methods</subject><subject>Female</subject><subject>fixel-based analysis</subject><subject>Humans</subject><subject>Klinisk medicin</subject><subject>Kurtosis</subject><subject>Magnetic resonance imaging</subject><subject>Male</subject><subject>Medical and Health Sciences</subject><subject>Medical imaging</subject><subject>Medicin och hälsovetenskap</subject><subject>memory</subject><subject>Middle Aged</subject><subject>Neurodegenerative diseases</subject><subject>Pathology</subject><subject>Positron emission</subject><subject>Radiologi och bildbehandling</subject><subject>Radiology, Nuclear Medicine and Medical Imaging</subject><subject>Substantia alba</subject><subject>Tau protein</subject><subject>tau Proteins - metabolism</subject><subject>Tensors</subject><subject>Thalamus</subject><subject>white matter</subject><subject>White Matter - diagnostic imaging</subject><subject>White Matter - pathology</subject><subject>β-Amyloid</subject><issn>0270-6474</issn><issn>1529-2401</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>D8T</sourceid><recordid>eNp1kt9v0zAQxyMEYmXwL0yReICXFP-284RK6WCoMKnbxKN1SS6rh5uUOBmUvx5HLRVD4uFk3933PjrL3yQ5o2RKJeNvPn1Z3Kwur-YXUyK5yRifMsLEo2QSu3nGBKGPkwlhmmRKaHGSPAvhjhCiCdVPkxNupJLM5JOkOnc_0WfvIGCVzhrwu-BCusJ7BB_SaxiyFXroY_Pr2vWYfoa-xy6dr6G5xZC6Jl1A53fpVQ9j3tbpzP9ao9tg9yqk713ASH6ePKkjDl8cztPk5nxxPf-YLS8_XMxny6wUIu8zyIUgGoypRFVKwLzQuSSyBsoLUWiqSZlLxmqtpSlAVcIYXiqjVAEliVV-mmR7bviB26Gw285toNvZFpw9lL7FG1ojpWIi6pf_1fthG6OIMQ7kiFIrIazSlFpRM2YLqKmVeRGXFTXROUTc2z0usjZYldj0HfgH1Iedxq3tbXtvKSWKG2oi4fWB0LXfBwy93bhQovfQYDsEywmnSjFjaJS-_Ed61w5d_MBRJaXkSnAeVWqvKrs2hA7r4zaU2NFI9mgkOxrJxspopDh49vdbjmN_nMN_AwxNxO0</recordid><startdate>20240501</startdate><enddate>20240501</enddate><creator>Ahmadi, Khazar</creator><creator>Pereira, Joana B</creator><creator>van Westen, Danielle</creator><creator>Pasternak, Ofer</creator><creator>Zhang, Fan</creator><creator>Nilsson, Markus</creator><creator>Stomrud, Erik</creator><creator>Spotorno, Nicola</creator><creator>Hansson, Oskar</creator><general>Society for Neuroscience</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>7QR</scope><scope>7TK</scope><scope>7U7</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope><scope>ADTPV</scope><scope>AOWAS</scope><scope>D95</scope><scope>D8T</scope><scope>ZZAVC</scope><orcidid>https://orcid.org/0000-0002-3371-6211</orcidid></search><sort><creationdate>20240501</creationdate><title>Fixel-Based Analysis Reveals Tau-Related White Matter Changes in Early Stages of Alzheimer's Disease</title><author>Ahmadi, Khazar ; Pereira, Joana B ; van Westen, Danielle ; Pasternak, Ofer ; Zhang, Fan ; Nilsson, Markus ; Stomrud, Erik ; Spotorno, Nicola ; Hansson, Oskar</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c449t-a94407a88d4dc5ae9b79505fa13b4b7170c9522f7758ba6d4883c6866bac0f773</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Abnormalities</topic><topic>Aged</topic><topic>Aged, 80 and over</topic><topic>Aggregation</topic><topic>Alzheimer Disease - diagnostic imaging</topic><topic>Alzheimer Disease - metabolism</topic><topic>Alzheimer Disease - pathology</topic><topic>Alzheimer's disease</topic><topic>Cingulum</topic><topic>Clinical Medicine</topic><topic>Cognition</topic><topic>Cognitive ability</topic><topic>Cognitive Dysfunction - diagnostic imaging</topic><topic>Cognitive Dysfunction - pathology</topic><topic>Degeneration</topic><topic>Diffusion</topic><topic>diffusion tensor imaging</topic><topic>Diffusion Tensor Imaging - methods</topic><topic>Female</topic><topic>fixel-based analysis</topic><topic>Humans</topic><topic>Klinisk medicin</topic><topic>Kurtosis</topic><topic>Magnetic resonance imaging</topic><topic>Male</topic><topic>Medical and Health Sciences</topic><topic>Medical imaging</topic><topic>Medicin och hälsovetenskap</topic><topic>memory</topic><topic>Middle Aged</topic><topic>Neurodegenerative diseases</topic><topic>Pathology</topic><topic>Positron emission</topic><topic>Radiologi och bildbehandling</topic><topic>Radiology, Nuclear Medicine and Medical Imaging</topic><topic>Substantia alba</topic><topic>Tau protein</topic><topic>tau Proteins - metabolism</topic><topic>Tensors</topic><topic>Thalamus</topic><topic>white matter</topic><topic>White Matter - diagnostic imaging</topic><topic>White Matter - pathology</topic><topic>β-Amyloid</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ahmadi, Khazar</creatorcontrib><creatorcontrib>Pereira, Joana B</creatorcontrib><creatorcontrib>van Westen, Danielle</creatorcontrib><creatorcontrib>Pasternak, Ofer</creatorcontrib><creatorcontrib>Zhang, Fan</creatorcontrib><creatorcontrib>Nilsson, Markus</creatorcontrib><creatorcontrib>Stomrud, Erik</creatorcontrib><creatorcontrib>Spotorno, Nicola</creatorcontrib><creatorcontrib>Hansson, Oskar</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>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>SwePub</collection><collection>SwePub Articles</collection><collection>SWEPUB Lunds universitet</collection><collection>SWEPUB Freely available online</collection><collection>SwePub Articles full text</collection><jtitle>The Journal of neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ahmadi, Khazar</au><au>Pereira, Joana B</au><au>van Westen, Danielle</au><au>Pasternak, Ofer</au><au>Zhang, Fan</au><au>Nilsson, Markus</au><au>Stomrud, Erik</au><au>Spotorno, Nicola</au><au>Hansson, Oskar</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Fixel-Based Analysis Reveals Tau-Related White Matter Changes in Early Stages of Alzheimer's Disease</atitle><jtitle>The Journal of neuroscience</jtitle><addtitle>J Neurosci</addtitle><date>2024-05-01</date><risdate>2024</risdate><volume>44</volume><issue>18</issue><spage>e0538232024</spage><pages>e0538232024-</pages><issn>0270-6474</issn><eissn>1529-2401</eissn><abstract>Several studies have shown white matter (WM) abnormalities in Alzheimer's disease (AD) using diffusion tensor imaging (DTI). Nonetheless, robust characterization of WM changes has been challenging due to the methodological limitations of DTI. We applied fixel-based analyses (FBA) to examine microscopic differences in fiber density (FD) and macroscopic changes in fiber cross-section (FC) in early stages of AD (
= 393, 212 females). FBA was also compared with DTI, free-water corrected (FW)-DTI and diffusion kurtosis imaging (DKI). We further investigated the correlation of FBA and tensor-derived metrics with AD pathology and cognition. FBA metrics were decreased in the entire cingulum bundle, uncinate fasciculus and anterior thalamic radiations in Aβ-positive patients with mild cognitive impairment compared to control groups. Metrics derived from DKI, and FW-DTI showed similar alterations whereas WM degeneration detected by DTI was more widespread. Tau-PET uptake in medial temporal regions was only correlated with reduced FC mainly in the parahippocampal cingulum in Aβ-positive individuals. This tau-related WM alteration was also associated with impaired memory. Despite the spatially extensive between-group differences in DTI-metrics, the link between WM and tau aggregation was only revealed using FBA metrics implying high sensitivity but low specificity of DTI-based measures in identifying subtle tau-related WM degeneration. No relationship was found between amyloid load and any diffusion-MRI measures. Our results indicate that early tau-related WM alterations in AD are due to macrostructural changes specifically captured by FBA metrics. Thus, future studies assessing the effects of AD pathology in WM tracts should consider using FBA metrics.</abstract><cop>United States</cop><pub>Society for Neuroscience</pub><pmid>38565289</pmid><doi>10.1523/JNEUROSCI.0538-23.2024</doi><orcidid>https://orcid.org/0000-0002-3371-6211</orcidid><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; SWEPUB Freely available online |
| subjects | Abnormalities Aged Aged, 80 and over Aggregation Alzheimer Disease - diagnostic imaging Alzheimer Disease - metabolism Alzheimer Disease - pathology Alzheimer's disease Cingulum Clinical Medicine Cognition Cognitive ability Cognitive Dysfunction - diagnostic imaging Cognitive Dysfunction - pathology Degeneration Diffusion diffusion tensor imaging Diffusion Tensor Imaging - methods Female fixel-based analysis Humans Klinisk medicin Kurtosis Magnetic resonance imaging Male Medical and Health Sciences Medical imaging Medicin och hälsovetenskap memory Middle Aged Neurodegenerative diseases Pathology Positron emission Radiologi och bildbehandling Radiology, Nuclear Medicine and Medical Imaging Substantia alba Tau protein tau Proteins - metabolism Tensors Thalamus white matter White Matter - diagnostic imaging White Matter - pathology β-Amyloid |
| title | Fixel-Based Analysis Reveals Tau-Related White Matter Changes in Early Stages of Alzheimer's Disease |
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