Noninvasive Characterization of Human Glymphatics and Meningeal Lymphatics in an in vivo Model of Blood–Brain Barrier Leakage
Objective To evaluate human glymphatics and meningeal lymphatics noninvasively. Methods This prospective study implemented 3‐dimensional (3D) isotropic contrast‐enhanced T2 fluid‐attenuated inversion recovery (CE‐T2‐FLAIR) imaging with a 3T magnetic resonance machine to study cerebral glymphatics an...
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| Veröffentlicht in: | Annals of neurology 2021-01, Vol.89 (1), p.111-124 |
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| creator | Wu, Chia‐Hung Lirng, Jiing‐Feng Ling, Yu‐Hsiang Wang, Yen‐Feng Wu, Hsiu‐Mei Fuh, Jong‐Ling Lin, Po‐Chen Wang, Shuu‐Jiun Chen, Shih‐Pin |
| description | Objective
To evaluate human glymphatics and meningeal lymphatics noninvasively.
Methods
This prospective study implemented 3‐dimensional (3D) isotropic contrast‐enhanced T2 fluid‐attenuated inversion recovery (CE‐T2‐FLAIR) imaging with a 3T magnetic resonance machine to study cerebral glymphatics and meningeal lymphatics in patients with reversible cerebral vasoconstriction syndrome (RCVS) with (n = 92) or without (n = 90) blood–brain barrier (BBB) disruption and a diseased control group with cluster headache (n = 35). The contrast agent gadobutrol (0.2mmol/kg [0.2ml/kg]) was administered intravenously in all study subjects.
Results
In total, 217 patients (182 RCVS, 35 cluster headache) were analyzed and separated into 2 groups based on the presence or absence of visible gadolinium (Gd) leakage. Para‐arterial tracer enrichment was clearly depicted in those with overt BBB disruption, while paravenous and parasinus meningeal contrast enrichment was evident in both groups. Paravenous and parasinus contrast enrichment remained in RCVS patients in the remission stage and in cluster headache patients, suggesting that these meningeal lymphatic channels were universal anatomical structures rather than being phase‐ or condition‐specific. Additionally, we demonstrated nodular leptomeningeal enhancement in 32.3% of participants, which might represent potential lymphatic reservoirs. Four selected RCVS patients who received consecutive contrasted 3D isotropic FLAIR imaging after gadobutrol administration showed that the Gd persisted for at least 54 minutes and was completely cleared within 18 hours.
Interpretation
This large‐scale in vivo study successfully demonstrated the putative human para‐arterial glymphatic transports and meningeal lymphatics by clear depiction of para‐arterial, parasinus, and paravenous meningeal contrast enrichment using high‐resolution 3D isotropic CE‐T2‐FLAIR imaging noninvasively; this technique may serve as a basis for further studies to delineate clinical relevance of glymphatic clearance. ANN NEUROL 2021;89:111–124 |
| doi_str_mv | 10.1002/ana.25928 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_2449263394</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2449263394</sourcerecordid><originalsourceid>FETCH-LOGICAL-c4198-d1efafdba25b2433e1f45baff7506d3b66c2a82c4b410a2621eb21af6405cb043</originalsourceid><addsrcrecordid>eNp1kc1OGzEURq2qqATaRV-gssQGFgP-m8nMMolKQErSTbse3Zm5BtMZO7UzqcIG3oE35ElwCFAJqRtfyd-5R1f6CPnK2SlnTJyBhVORFiL_QAY8lTzJhSo-kgGTmUpSLtU-OQjhhjFWZJx9IvtSMslEOhyQu4Wzxq4hmDXSyTV4qFfozS2sjLPUaXrRd2DptN10y-v4WQcKtqFzjFtXCC2d_QuMjdn2XZu1o3PXYLs1jFvnmsf7h7GHmI3Be4OezhB-wxV-Jnsa2oBfXuYh-XX-_efkIpn9mF5ORrOkVrzIk4ajBt1UINJKKCmRa5VWoPUwZVkjqyyrBeSiVpXiDEQmOFaCg84US-uKKXlIjnfepXd_egyrsjOhxrYFi64PpVCqEJmUxRY9eofeuN7beF2khkwVUso8Uic7qvYuBI-6XHrTgd-UnJXbVsrYSvncSmS_vRj7qsPmjXytIQJnO-CvaXHzf1M5Wox2yic7A5ez</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2470493338</pqid></control><display><type>article</type><title>Noninvasive Characterization of Human Glymphatics and Meningeal Lymphatics in an in vivo Model of Blood–Brain Barrier Leakage</title><source>MEDLINE</source><source>Access via Wiley Online Library</source><creator>Wu, Chia‐Hung ; Lirng, Jiing‐Feng ; Ling, Yu‐Hsiang ; Wang, Yen‐Feng ; Wu, Hsiu‐Mei ; Fuh, Jong‐Ling ; Lin, Po‐Chen ; Wang, Shuu‐Jiun ; Chen, Shih‐Pin</creator><creatorcontrib>Wu, Chia‐Hung ; Lirng, Jiing‐Feng ; Ling, Yu‐Hsiang ; Wang, Yen‐Feng ; Wu, Hsiu‐Mei ; Fuh, Jong‐Ling ; Lin, Po‐Chen ; Wang, Shuu‐Jiun ; Chen, Shih‐Pin</creatorcontrib><description>Objective
To evaluate human glymphatics and meningeal lymphatics noninvasively.
Methods
This prospective study implemented 3‐dimensional (3D) isotropic contrast‐enhanced T2 fluid‐attenuated inversion recovery (CE‐T2‐FLAIR) imaging with a 3T magnetic resonance machine to study cerebral glymphatics and meningeal lymphatics in patients with reversible cerebral vasoconstriction syndrome (RCVS) with (n = 92) or without (n = 90) blood–brain barrier (BBB) disruption and a diseased control group with cluster headache (n = 35). The contrast agent gadobutrol (0.2mmol/kg [0.2ml/kg]) was administered intravenously in all study subjects.
Results
In total, 217 patients (182 RCVS, 35 cluster headache) were analyzed and separated into 2 groups based on the presence or absence of visible gadolinium (Gd) leakage. Para‐arterial tracer enrichment was clearly depicted in those with overt BBB disruption, while paravenous and parasinus meningeal contrast enrichment was evident in both groups. Paravenous and parasinus contrast enrichment remained in RCVS patients in the remission stage and in cluster headache patients, suggesting that these meningeal lymphatic channels were universal anatomical structures rather than being phase‐ or condition‐specific. Additionally, we demonstrated nodular leptomeningeal enhancement in 32.3% of participants, which might represent potential lymphatic reservoirs. Four selected RCVS patients who received consecutive contrasted 3D isotropic FLAIR imaging after gadobutrol administration showed that the Gd persisted for at least 54 minutes and was completely cleared within 18 hours.
Interpretation
This large‐scale in vivo study successfully demonstrated the putative human para‐arterial glymphatic transports and meningeal lymphatics by clear depiction of para‐arterial, parasinus, and paravenous meningeal contrast enrichment using high‐resolution 3D isotropic CE‐T2‐FLAIR imaging noninvasively; this technique may serve as a basis for further studies to delineate clinical relevance of glymphatic clearance. ANN NEUROL 2021;89:111–124</description><identifier>ISSN: 0364-5134</identifier><identifier>EISSN: 1531-8249</identifier><identifier>DOI: 10.1002/ana.25928</identifier><identifier>PMID: 33030257</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>Adult ; Blood-brain barrier ; Blood-Brain Barrier - pathology ; Blood-Brain Barrier - physiopathology ; Cerebrovascular Disorders - pathology ; Cerebrovascular Disorders - physiopathology ; Clusters ; Contrast agents ; Contrast Media - pharmacology ; Disruption ; Enrichment ; Female ; Gadolinium ; Headache ; Headaches ; Humans ; In vivo methods and tests ; Leakage ; Magnetic resonance ; Magnetic resonance imaging ; Magnetic Resonance Imaging - methods ; Male ; Medical imaging ; Meninges ; Meninges - pathology ; Meninges - physiopathology ; Middle Aged ; Neuroimaging ; Organometallic Compounds - metabolism ; Remission ; Vasoconstriction</subject><ispartof>Annals of neurology, 2021-01, Vol.89 (1), p.111-124</ispartof><rights>2020 American Neurological Association</rights><rights>2020 American Neurological Association.</rights><rights>2021 American Neurological Association</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4198-d1efafdba25b2433e1f45baff7506d3b66c2a82c4b410a2621eb21af6405cb043</citedby><cites>FETCH-LOGICAL-c4198-d1efafdba25b2433e1f45baff7506d3b66c2a82c4b410a2621eb21af6405cb043</cites><orcidid>0000-0003-3492-9902 ; 0000-0003-1723-4797</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%2Fana.25928$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fana.25928$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>315,781,785,1418,27926,27927,45576,45577</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33030257$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wu, Chia‐Hung</creatorcontrib><creatorcontrib>Lirng, Jiing‐Feng</creatorcontrib><creatorcontrib>Ling, Yu‐Hsiang</creatorcontrib><creatorcontrib>Wang, Yen‐Feng</creatorcontrib><creatorcontrib>Wu, Hsiu‐Mei</creatorcontrib><creatorcontrib>Fuh, Jong‐Ling</creatorcontrib><creatorcontrib>Lin, Po‐Chen</creatorcontrib><creatorcontrib>Wang, Shuu‐Jiun</creatorcontrib><creatorcontrib>Chen, Shih‐Pin</creatorcontrib><title>Noninvasive Characterization of Human Glymphatics and Meningeal Lymphatics in an in vivo Model of Blood–Brain Barrier Leakage</title><title>Annals of neurology</title><addtitle>Ann Neurol</addtitle><description>Objective
To evaluate human glymphatics and meningeal lymphatics noninvasively.
Methods
This prospective study implemented 3‐dimensional (3D) isotropic contrast‐enhanced T2 fluid‐attenuated inversion recovery (CE‐T2‐FLAIR) imaging with a 3T magnetic resonance machine to study cerebral glymphatics and meningeal lymphatics in patients with reversible cerebral vasoconstriction syndrome (RCVS) with (n = 92) or without (n = 90) blood–brain barrier (BBB) disruption and a diseased control group with cluster headache (n = 35). The contrast agent gadobutrol (0.2mmol/kg [0.2ml/kg]) was administered intravenously in all study subjects.
Results
In total, 217 patients (182 RCVS, 35 cluster headache) were analyzed and separated into 2 groups based on the presence or absence of visible gadolinium (Gd) leakage. Para‐arterial tracer enrichment was clearly depicted in those with overt BBB disruption, while paravenous and parasinus meningeal contrast enrichment was evident in both groups. Paravenous and parasinus contrast enrichment remained in RCVS patients in the remission stage and in cluster headache patients, suggesting that these meningeal lymphatic channels were universal anatomical structures rather than being phase‐ or condition‐specific. Additionally, we demonstrated nodular leptomeningeal enhancement in 32.3% of participants, which might represent potential lymphatic reservoirs. Four selected RCVS patients who received consecutive contrasted 3D isotropic FLAIR imaging after gadobutrol administration showed that the Gd persisted for at least 54 minutes and was completely cleared within 18 hours.
Interpretation
This large‐scale in vivo study successfully demonstrated the putative human para‐arterial glymphatic transports and meningeal lymphatics by clear depiction of para‐arterial, parasinus, and paravenous meningeal contrast enrichment using high‐resolution 3D isotropic CE‐T2‐FLAIR imaging noninvasively; this technique may serve as a basis for further studies to delineate clinical relevance of glymphatic clearance. ANN NEUROL 2021;89:111–124</description><subject>Adult</subject><subject>Blood-brain barrier</subject><subject>Blood-Brain Barrier - pathology</subject><subject>Blood-Brain Barrier - physiopathology</subject><subject>Cerebrovascular Disorders - pathology</subject><subject>Cerebrovascular Disorders - physiopathology</subject><subject>Clusters</subject><subject>Contrast agents</subject><subject>Contrast Media - pharmacology</subject><subject>Disruption</subject><subject>Enrichment</subject><subject>Female</subject><subject>Gadolinium</subject><subject>Headache</subject><subject>Headaches</subject><subject>Humans</subject><subject>In vivo methods and tests</subject><subject>Leakage</subject><subject>Magnetic resonance</subject><subject>Magnetic resonance imaging</subject><subject>Magnetic Resonance Imaging - methods</subject><subject>Male</subject><subject>Medical imaging</subject><subject>Meninges</subject><subject>Meninges - pathology</subject><subject>Meninges - physiopathology</subject><subject>Middle Aged</subject><subject>Neuroimaging</subject><subject>Organometallic Compounds - metabolism</subject><subject>Remission</subject><subject>Vasoconstriction</subject><issn>0364-5134</issn><issn>1531-8249</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kc1OGzEURq2qqATaRV-gssQGFgP-m8nMMolKQErSTbse3Zm5BtMZO7UzqcIG3oE35ElwCFAJqRtfyd-5R1f6CPnK2SlnTJyBhVORFiL_QAY8lTzJhSo-kgGTmUpSLtU-OQjhhjFWZJx9IvtSMslEOhyQu4Wzxq4hmDXSyTV4qFfozS2sjLPUaXrRd2DptN10y-v4WQcKtqFzjFtXCC2d_QuMjdn2XZu1o3PXYLs1jFvnmsf7h7GHmI3Be4OezhB-wxV-Jnsa2oBfXuYh-XX-_efkIpn9mF5ORrOkVrzIk4ajBt1UINJKKCmRa5VWoPUwZVkjqyyrBeSiVpXiDEQmOFaCg84US-uKKXlIjnfepXd_egyrsjOhxrYFi64PpVCqEJmUxRY9eofeuN7beF2khkwVUso8Uic7qvYuBI-6XHrTgd-UnJXbVsrYSvncSmS_vRj7qsPmjXytIQJnO-CvaXHzf1M5Wox2yic7A5ez</recordid><startdate>202101</startdate><enddate>202101</enddate><creator>Wu, Chia‐Hung</creator><creator>Lirng, Jiing‐Feng</creator><creator>Ling, Yu‐Hsiang</creator><creator>Wang, Yen‐Feng</creator><creator>Wu, Hsiu‐Mei</creator><creator>Fuh, Jong‐Ling</creator><creator>Lin, Po‐Chen</creator><creator>Wang, Shuu‐Jiun</creator><creator>Chen, Shih‐Pin</creator><general>John Wiley & Sons, Inc</general><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>7TK</scope><scope>7U7</scope><scope>C1K</scope><scope>K9.</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0003-3492-9902</orcidid><orcidid>https://orcid.org/0000-0003-1723-4797</orcidid></search><sort><creationdate>202101</creationdate><title>Noninvasive Characterization of Human Glymphatics and Meningeal Lymphatics in an in vivo Model of Blood–Brain Barrier Leakage</title><author>Wu, Chia‐Hung ; Lirng, Jiing‐Feng ; Ling, Yu‐Hsiang ; Wang, Yen‐Feng ; Wu, Hsiu‐Mei ; Fuh, Jong‐Ling ; Lin, Po‐Chen ; Wang, Shuu‐Jiun ; Chen, Shih‐Pin</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4198-d1efafdba25b2433e1f45baff7506d3b66c2a82c4b410a2621eb21af6405cb043</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Adult</topic><topic>Blood-brain barrier</topic><topic>Blood-Brain Barrier - pathology</topic><topic>Blood-Brain Barrier - physiopathology</topic><topic>Cerebrovascular Disorders - pathology</topic><topic>Cerebrovascular Disorders - physiopathology</topic><topic>Clusters</topic><topic>Contrast agents</topic><topic>Contrast Media - pharmacology</topic><topic>Disruption</topic><topic>Enrichment</topic><topic>Female</topic><topic>Gadolinium</topic><topic>Headache</topic><topic>Headaches</topic><topic>Humans</topic><topic>In vivo methods and tests</topic><topic>Leakage</topic><topic>Magnetic resonance</topic><topic>Magnetic resonance imaging</topic><topic>Magnetic Resonance Imaging - methods</topic><topic>Male</topic><topic>Medical imaging</topic><topic>Meninges</topic><topic>Meninges - pathology</topic><topic>Meninges - physiopathology</topic><topic>Middle Aged</topic><topic>Neuroimaging</topic><topic>Organometallic Compounds - metabolism</topic><topic>Remission</topic><topic>Vasoconstriction</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wu, Chia‐Hung</creatorcontrib><creatorcontrib>Lirng, Jiing‐Feng</creatorcontrib><creatorcontrib>Ling, Yu‐Hsiang</creatorcontrib><creatorcontrib>Wang, Yen‐Feng</creatorcontrib><creatorcontrib>Wu, Hsiu‐Mei</creatorcontrib><creatorcontrib>Fuh, Jong‐Ling</creatorcontrib><creatorcontrib>Lin, Po‐Chen</creatorcontrib><creatorcontrib>Wang, Shuu‐Jiun</creatorcontrib><creatorcontrib>Chen, Shih‐Pin</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>Toxicology Abstracts</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><jtitle>Annals of neurology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wu, Chia‐Hung</au><au>Lirng, Jiing‐Feng</au><au>Ling, Yu‐Hsiang</au><au>Wang, Yen‐Feng</au><au>Wu, Hsiu‐Mei</au><au>Fuh, Jong‐Ling</au><au>Lin, Po‐Chen</au><au>Wang, Shuu‐Jiun</au><au>Chen, Shih‐Pin</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Noninvasive Characterization of Human Glymphatics and Meningeal Lymphatics in an in vivo Model of Blood–Brain Barrier Leakage</atitle><jtitle>Annals of neurology</jtitle><addtitle>Ann Neurol</addtitle><date>2021-01</date><risdate>2021</risdate><volume>89</volume><issue>1</issue><spage>111</spage><epage>124</epage><pages>111-124</pages><issn>0364-5134</issn><eissn>1531-8249</eissn><abstract>Objective
To evaluate human glymphatics and meningeal lymphatics noninvasively.
Methods
This prospective study implemented 3‐dimensional (3D) isotropic contrast‐enhanced T2 fluid‐attenuated inversion recovery (CE‐T2‐FLAIR) imaging with a 3T magnetic resonance machine to study cerebral glymphatics and meningeal lymphatics in patients with reversible cerebral vasoconstriction syndrome (RCVS) with (n = 92) or without (n = 90) blood–brain barrier (BBB) disruption and a diseased control group with cluster headache (n = 35). The contrast agent gadobutrol (0.2mmol/kg [0.2ml/kg]) was administered intravenously in all study subjects.
Results
In total, 217 patients (182 RCVS, 35 cluster headache) were analyzed and separated into 2 groups based on the presence or absence of visible gadolinium (Gd) leakage. Para‐arterial tracer enrichment was clearly depicted in those with overt BBB disruption, while paravenous and parasinus meningeal contrast enrichment was evident in both groups. Paravenous and parasinus contrast enrichment remained in RCVS patients in the remission stage and in cluster headache patients, suggesting that these meningeal lymphatic channels were universal anatomical structures rather than being phase‐ or condition‐specific. Additionally, we demonstrated nodular leptomeningeal enhancement in 32.3% of participants, which might represent potential lymphatic reservoirs. Four selected RCVS patients who received consecutive contrasted 3D isotropic FLAIR imaging after gadobutrol administration showed that the Gd persisted for at least 54 minutes and was completely cleared within 18 hours.
Interpretation
This large‐scale in vivo study successfully demonstrated the putative human para‐arterial glymphatic transports and meningeal lymphatics by clear depiction of para‐arterial, parasinus, and paravenous meningeal contrast enrichment using high‐resolution 3D isotropic CE‐T2‐FLAIR imaging noninvasively; this technique may serve as a basis for further studies to delineate clinical relevance of glymphatic clearance. ANN NEUROL 2021;89:111–124</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><pmid>33030257</pmid><doi>10.1002/ana.25928</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0003-3492-9902</orcidid><orcidid>https://orcid.org/0000-0003-1723-4797</orcidid></addata></record> |
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| ispartof | Annals of neurology, 2021-01, Vol.89 (1), p.111-124 |
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| language | eng |
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| source | MEDLINE; Access via Wiley Online Library |
| subjects | Adult Blood-brain barrier Blood-Brain Barrier - pathology Blood-Brain Barrier - physiopathology Cerebrovascular Disorders - pathology Cerebrovascular Disorders - physiopathology Clusters Contrast agents Contrast Media - pharmacology Disruption Enrichment Female Gadolinium Headache Headaches Humans In vivo methods and tests Leakage Magnetic resonance Magnetic resonance imaging Magnetic Resonance Imaging - methods Male Medical imaging Meninges Meninges - pathology Meninges - physiopathology Middle Aged Neuroimaging Organometallic Compounds - metabolism Remission Vasoconstriction |
| title | Noninvasive Characterization of Human Glymphatics and Meningeal Lymphatics in an in vivo Model of Blood–Brain Barrier Leakage |
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