Evaluation of Cognitive Deficits and Structural Hippocampal Damage in Encephalitis With Leucine-Rich, Glioma-Inactivated 1 Antibodies
IMPORTANCE: Limbic encephalitis with leucine-rich, glioma-inactivated 1 (LGI1) antibodies is one of the most frequent variants of autoimmune encephalitis with antibodies targeting neuronal surface antigens. However, the neuroimaging pattern and long-term cognitive outcome are not well understood. OB...
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| Veröffentlicht in: | JAMA neurology 2017-01, Vol.74 (1), p.50-59 |
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| creator | Finke, Carsten Prüss, Harald Heine, Josephine Reuter, Sigrid Kopp, Ute A Wegner, Florian Then Bergh, Florian Koch, Sebastian Jansen, Olav Münte, Thomas Deuschl, Günther Ruprecht, Klemens Stöcker, Winfried Wandinger, Klaus-Peter Paul, Friedemann Bartsch, Thorsten |
| description | IMPORTANCE: Limbic encephalitis with leucine-rich, glioma-inactivated 1 (LGI1) antibodies is one of the most frequent variants of autoimmune encephalitis with antibodies targeting neuronal surface antigens. However, the neuroimaging pattern and long-term cognitive outcome are not well understood. OBJECTIVE: To study cognitive outcome and structural magnetic resonance imaging (MRI) alterations in patients with anti-LGI1 encephalitis. DESIGN, SETTING, AND PARTICIPANTS: A cross-sectional study was conducted at the Departments of Neurology at Charité-Universitätsmedizin Berlin and University Hospital Schleswig-Holstein, Kiel, Germany. Data on 30 patients with anti-LGI1 encephalitis and 27 healthy control individuals matched for age, sex, and educational level were collected from June 1, 2013, through February 28, 2015. MAIN OUTCOMES AND MEASURES: Clinical assessment, cognitive testing, and high-resolution MRI data, including whole-brain, hippocampal and basal ganglia volumetry; white matter integrity (diffusion tensor imaging); gray matter density (voxel-based morphometry); and hippocampal microstructural integrity (mean diffusivity and fractional anisotropy). RESULTS: Of the 30 patients included in the study, 19 were male (63%); mean (SD) age was 65.7 (12.3) years. Patients with anti-LGI1 encephalitis had incomplete recovery with significant and persisting verbal (mean [SE] Rey Auditory Verbal Learning Test [RAVLT], delayed recall: patients, 6.52 [1.05]; controls, 11.78 [0.56], P |
| doi_str_mv | 10.1001/jamaneurol.2016.4226 |
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However, the neuroimaging pattern and long-term cognitive outcome are not well understood. OBJECTIVE: To study cognitive outcome and structural magnetic resonance imaging (MRI) alterations in patients with anti-LGI1 encephalitis. DESIGN, SETTING, AND PARTICIPANTS: A cross-sectional study was conducted at the Departments of Neurology at Charité-Universitätsmedizin Berlin and University Hospital Schleswig-Holstein, Kiel, Germany. Data on 30 patients with anti-LGI1 encephalitis and 27 healthy control individuals matched for age, sex, and educational level were collected from June 1, 2013, through February 28, 2015. MAIN OUTCOMES AND MEASURES: Clinical assessment, cognitive testing, and high-resolution MRI data, including whole-brain, hippocampal and basal ganglia volumetry; white matter integrity (diffusion tensor imaging); gray matter density (voxel-based morphometry); and hippocampal microstructural integrity (mean diffusivity and fractional anisotropy). RESULTS: Of the 30 patients included in the study, 19 were male (63%); mean (SD) age was 65.7 (12.3) years. Patients with anti-LGI1 encephalitis had incomplete recovery with significant and persisting verbal (mean [SE] Rey Auditory Verbal Learning Test [RAVLT], delayed recall: patients, 6.52 [1.05]; controls, 11.78 [0.56], P < .001) and visuospatial (Rey-Osterrieth Complex Figure Test [ROCF], delayed recall: patients, 16.0 [1.96]; controls, 25.86 [1.24]; P < .001) memory deficits. These deficits were accompanied by pronounced hippocampal atrophy, including subfields cornu ammonis 2/3 (CA2/3) and CA4/dentate gyrus (DG), as well as impaired hippocampal microstructural integrity. Higher disease severity correlated with larger verbal memory deficits (RAVLT delayed recall, r = −0.40; P = .049), decreased volumes of left hippocampus (r = −0.47; P = .02) and left CA2/3 (r = −0.41; P = .04) and CA4/DG (r = −0.43; P = .03) subfields, and impaired left hippocampal microstructural integrity (r = 0.47; P = .01). In turn, decreased volume of the left CA2/3 subfield (RAVLT delayed recall, r = 0.40; P = .047) and impaired left hippocampal microstructural integrity (RAVLT recognition, r = −0.41; P = .04) correlated with verbal memory deficits. Basal ganglia MRI signal abnormalities were observed in only 1 patient, but a longer duration of faciobrachial dystonic seizures correlated with a reduction of pallidum volume (r = −0.71; P = .03). In contrast, no abnormalities of cortical gray matter or white matter were found. The latency between disease onset and initiation of immunotherapy was significantly correlated with verbal (RAVLT recall after interference, r = −0.48; P = .02) and visuospatial (ROCF delayed recall, r = −0.46; P = .03) memory deficits. CONCLUSIONS AND RELEVANCE: Anti-LGI1 encephalitis is associated with cognitive deficits and disability as a result of structural damage to the hippocampal memory system. This damage might be prevented by early immunotherapy.</description><identifier>ISSN: 2168-6149</identifier><identifier>EISSN: 2168-6157</identifier><identifier>DOI: 10.1001/jamaneurol.2016.4226</identifier><identifier>PMID: 27893017</identifier><language>eng</language><publisher>United States: American Medical Association</publisher><subject>Aged ; Autoantibodies - blood ; Basal Ganglia - diagnostic imaging ; Cognition Disorders - etiology ; Cross-Sectional Studies ; Disability Evaluation ; Female ; HEK293 Cells - metabolism ; Hippocampus - diagnostic imaging ; Humans ; Immunotherapy ; Intracellular Signaling Peptides and Proteins ; Limbic Encephalitis - blood ; Limbic Encephalitis - complications ; Limbic Encephalitis - diagnostic imaging ; Limbic Encephalitis - therapy ; Longitudinal Studies ; Magnetic Resonance Imaging ; Male ; Middle Aged ; Neuropsychological Tests ; Proteins - immunology ; Retrospective Studies</subject><ispartof>JAMA neurology, 2017-01, Vol.74 (1), p.50-59</ispartof><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-a405t-406b1c74dcdf932bc64e8375e58264161d3a3c13dff9b540308cb408c2ac7f943</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://jamanetwork.com/journals/jamaneurology/articlepdf/10.1001/jamaneurol.2016.4226$$EPDF$$P50$$Gama$$H</linktopdf><linktohtml>$$Uhttps://jamanetwork.com/journals/jamaneurology/fullarticle/10.1001/jamaneurol.2016.4226$$EHTML$$P50$$Gama$$H</linktohtml><link.rule.ids>64,314,776,780,3327,27901,27902,76231,76234</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27893017$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Finke, Carsten</creatorcontrib><creatorcontrib>Prüss, Harald</creatorcontrib><creatorcontrib>Heine, Josephine</creatorcontrib><creatorcontrib>Reuter, Sigrid</creatorcontrib><creatorcontrib>Kopp, Ute A</creatorcontrib><creatorcontrib>Wegner, Florian</creatorcontrib><creatorcontrib>Then Bergh, Florian</creatorcontrib><creatorcontrib>Koch, Sebastian</creatorcontrib><creatorcontrib>Jansen, Olav</creatorcontrib><creatorcontrib>Münte, Thomas</creatorcontrib><creatorcontrib>Deuschl, Günther</creatorcontrib><creatorcontrib>Ruprecht, Klemens</creatorcontrib><creatorcontrib>Stöcker, Winfried</creatorcontrib><creatorcontrib>Wandinger, Klaus-Peter</creatorcontrib><creatorcontrib>Paul, Friedemann</creatorcontrib><creatorcontrib>Bartsch, Thorsten</creatorcontrib><title>Evaluation of Cognitive Deficits and Structural Hippocampal Damage in Encephalitis With Leucine-Rich, Glioma-Inactivated 1 Antibodies</title><title>JAMA neurology</title><addtitle>JAMA Neurol</addtitle><description>IMPORTANCE: Limbic encephalitis with leucine-rich, glioma-inactivated 1 (LGI1) antibodies is one of the most frequent variants of autoimmune encephalitis with antibodies targeting neuronal surface antigens. However, the neuroimaging pattern and long-term cognitive outcome are not well understood. OBJECTIVE: To study cognitive outcome and structural magnetic resonance imaging (MRI) alterations in patients with anti-LGI1 encephalitis. DESIGN, SETTING, AND PARTICIPANTS: A cross-sectional study was conducted at the Departments of Neurology at Charité-Universitätsmedizin Berlin and University Hospital Schleswig-Holstein, Kiel, Germany. Data on 30 patients with anti-LGI1 encephalitis and 27 healthy control individuals matched for age, sex, and educational level were collected from June 1, 2013, through February 28, 2015. MAIN OUTCOMES AND MEASURES: Clinical assessment, cognitive testing, and high-resolution MRI data, including whole-brain, hippocampal and basal ganglia volumetry; white matter integrity (diffusion tensor imaging); gray matter density (voxel-based morphometry); and hippocampal microstructural integrity (mean diffusivity and fractional anisotropy). RESULTS: Of the 30 patients included in the study, 19 were male (63%); mean (SD) age was 65.7 (12.3) years. Patients with anti-LGI1 encephalitis had incomplete recovery with significant and persisting verbal (mean [SE] Rey Auditory Verbal Learning Test [RAVLT], delayed recall: patients, 6.52 [1.05]; controls, 11.78 [0.56], P < .001) and visuospatial (Rey-Osterrieth Complex Figure Test [ROCF], delayed recall: patients, 16.0 [1.96]; controls, 25.86 [1.24]; P < .001) memory deficits. These deficits were accompanied by pronounced hippocampal atrophy, including subfields cornu ammonis 2/3 (CA2/3) and CA4/dentate gyrus (DG), as well as impaired hippocampal microstructural integrity. Higher disease severity correlated with larger verbal memory deficits (RAVLT delayed recall, r = −0.40; P = .049), decreased volumes of left hippocampus (r = −0.47; P = .02) and left CA2/3 (r = −0.41; P = .04) and CA4/DG (r = −0.43; P = .03) subfields, and impaired left hippocampal microstructural integrity (r = 0.47; P = .01). In turn, decreased volume of the left CA2/3 subfield (RAVLT delayed recall, r = 0.40; P = .047) and impaired left hippocampal microstructural integrity (RAVLT recognition, r = −0.41; P = .04) correlated with verbal memory deficits. Basal ganglia MRI signal abnormalities were observed in only 1 patient, but a longer duration of faciobrachial dystonic seizures correlated with a reduction of pallidum volume (r = −0.71; P = .03). In contrast, no abnormalities of cortical gray matter or white matter were found. The latency between disease onset and initiation of immunotherapy was significantly correlated with verbal (RAVLT recall after interference, r = −0.48; P = .02) and visuospatial (ROCF delayed recall, r = −0.46; P = .03) memory deficits. CONCLUSIONS AND RELEVANCE: Anti-LGI1 encephalitis is associated with cognitive deficits and disability as a result of structural damage to the hippocampal memory system. This damage might be prevented by early immunotherapy.</description><subject>Aged</subject><subject>Autoantibodies - blood</subject><subject>Basal Ganglia - diagnostic imaging</subject><subject>Cognition Disorders - etiology</subject><subject>Cross-Sectional Studies</subject><subject>Disability Evaluation</subject><subject>Female</subject><subject>HEK293 Cells - metabolism</subject><subject>Hippocampus - diagnostic imaging</subject><subject>Humans</subject><subject>Immunotherapy</subject><subject>Intracellular Signaling Peptides and Proteins</subject><subject>Limbic Encephalitis - blood</subject><subject>Limbic Encephalitis - complications</subject><subject>Limbic Encephalitis - diagnostic imaging</subject><subject>Limbic Encephalitis - therapy</subject><subject>Longitudinal Studies</subject><subject>Magnetic Resonance Imaging</subject><subject>Male</subject><subject>Middle Aged</subject><subject>Neuropsychological Tests</subject><subject>Proteins - immunology</subject><subject>Retrospective Studies</subject><issn>2168-6149</issn><issn>2168-6157</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkd1OwyAYhonRqJm7AWMMhx7YCYVSemi2uS1ZYuJPPGwopRtLC7XQJV6A9y3L5jyVBPgSnveD8ABwg9EII4QfNqIRRvWdrUcxwmxE45idgMsYMx4xnKSnx5pmF2Do3AaFwRGihJ6DizjlGUE4vQTf062oe-G1NdBWcGxXRnu9VXCiKi21d1CYEr76rpe-70QN57ptrRRNG-pJeMVKQW3g1EjVrkUdsg5-aL-GS9VLbVT0ouX6Hs5qbRsRLYyQobvwqoQYPhqvC1tq5a7AWSVqp4aHfQDen6Zv43m0fJ4txo_LSFCU-IgiVmCZ0lKWVUbiQjKqOEkTlfCYUcxwSQSRmJRVlRUJRQRxWdCwxEKmVUbJANzt-7ad_eyV83mjnVR1HT7T9i7HnHGCspTjf6CUkiRhmASU7lHZWec6VeVtpxvRfeUY5Ttd-Z-ufKcr3-kKsdvDDX3RqPIY-pUTgOs9ENJ_pwlnYZIfp9acdw</recordid><startdate>20170101</startdate><enddate>20170101</enddate><creator>Finke, Carsten</creator><creator>Prüss, Harald</creator><creator>Heine, Josephine</creator><creator>Reuter, Sigrid</creator><creator>Kopp, Ute A</creator><creator>Wegner, Florian</creator><creator>Then Bergh, Florian</creator><creator>Koch, Sebastian</creator><creator>Jansen, Olav</creator><creator>Münte, Thomas</creator><creator>Deuschl, Günther</creator><creator>Ruprecht, Klemens</creator><creator>Stöcker, Winfried</creator><creator>Wandinger, Klaus-Peter</creator><creator>Paul, Friedemann</creator><creator>Bartsch, Thorsten</creator><general>American Medical Association</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>7X8</scope><scope>7TK</scope></search><sort><creationdate>20170101</creationdate><title>Evaluation of Cognitive Deficits and Structural Hippocampal Damage in Encephalitis With Leucine-Rich, Glioma-Inactivated 1 Antibodies</title><author>Finke, Carsten ; Prüss, Harald ; Heine, Josephine ; Reuter, Sigrid ; Kopp, Ute A ; Wegner, Florian ; Then Bergh, Florian ; Koch, Sebastian ; Jansen, Olav ; Münte, Thomas ; Deuschl, Günther ; Ruprecht, Klemens ; Stöcker, Winfried ; Wandinger, Klaus-Peter ; Paul, Friedemann ; Bartsch, Thorsten</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a405t-406b1c74dcdf932bc64e8375e58264161d3a3c13dff9b540308cb408c2ac7f943</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Aged</topic><topic>Autoantibodies - blood</topic><topic>Basal Ganglia - diagnostic imaging</topic><topic>Cognition Disorders - etiology</topic><topic>Cross-Sectional Studies</topic><topic>Disability Evaluation</topic><topic>Female</topic><topic>HEK293 Cells - metabolism</topic><topic>Hippocampus - diagnostic imaging</topic><topic>Humans</topic><topic>Immunotherapy</topic><topic>Intracellular Signaling Peptides and Proteins</topic><topic>Limbic Encephalitis - blood</topic><topic>Limbic Encephalitis - complications</topic><topic>Limbic Encephalitis - diagnostic imaging</topic><topic>Limbic Encephalitis - therapy</topic><topic>Longitudinal Studies</topic><topic>Magnetic Resonance Imaging</topic><topic>Male</topic><topic>Middle Aged</topic><topic>Neuropsychological Tests</topic><topic>Proteins - immunology</topic><topic>Retrospective Studies</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Finke, Carsten</creatorcontrib><creatorcontrib>Prüss, Harald</creatorcontrib><creatorcontrib>Heine, Josephine</creatorcontrib><creatorcontrib>Reuter, Sigrid</creatorcontrib><creatorcontrib>Kopp, Ute A</creatorcontrib><creatorcontrib>Wegner, Florian</creatorcontrib><creatorcontrib>Then Bergh, Florian</creatorcontrib><creatorcontrib>Koch, Sebastian</creatorcontrib><creatorcontrib>Jansen, Olav</creatorcontrib><creatorcontrib>Münte, Thomas</creatorcontrib><creatorcontrib>Deuschl, Günther</creatorcontrib><creatorcontrib>Ruprecht, Klemens</creatorcontrib><creatorcontrib>Stöcker, Winfried</creatorcontrib><creatorcontrib>Wandinger, Klaus-Peter</creatorcontrib><creatorcontrib>Paul, Friedemann</creatorcontrib><creatorcontrib>Bartsch, Thorsten</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Neurosciences Abstracts</collection><jtitle>JAMA neurology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Finke, Carsten</au><au>Prüss, Harald</au><au>Heine, Josephine</au><au>Reuter, Sigrid</au><au>Kopp, Ute A</au><au>Wegner, Florian</au><au>Then Bergh, Florian</au><au>Koch, Sebastian</au><au>Jansen, Olav</au><au>Münte, Thomas</au><au>Deuschl, Günther</au><au>Ruprecht, Klemens</au><au>Stöcker, Winfried</au><au>Wandinger, Klaus-Peter</au><au>Paul, Friedemann</au><au>Bartsch, Thorsten</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Evaluation of Cognitive Deficits and Structural Hippocampal Damage in Encephalitis With Leucine-Rich, Glioma-Inactivated 1 Antibodies</atitle><jtitle>JAMA neurology</jtitle><addtitle>JAMA Neurol</addtitle><date>2017-01-01</date><risdate>2017</risdate><volume>74</volume><issue>1</issue><spage>50</spage><epage>59</epage><pages>50-59</pages><issn>2168-6149</issn><eissn>2168-6157</eissn><abstract>IMPORTANCE: Limbic encephalitis with leucine-rich, glioma-inactivated 1 (LGI1) antibodies is one of the most frequent variants of autoimmune encephalitis with antibodies targeting neuronal surface antigens. However, the neuroimaging pattern and long-term cognitive outcome are not well understood. OBJECTIVE: To study cognitive outcome and structural magnetic resonance imaging (MRI) alterations in patients with anti-LGI1 encephalitis. DESIGN, SETTING, AND PARTICIPANTS: A cross-sectional study was conducted at the Departments of Neurology at Charité-Universitätsmedizin Berlin and University Hospital Schleswig-Holstein, Kiel, Germany. Data on 30 patients with anti-LGI1 encephalitis and 27 healthy control individuals matched for age, sex, and educational level were collected from June 1, 2013, through February 28, 2015. MAIN OUTCOMES AND MEASURES: Clinical assessment, cognitive testing, and high-resolution MRI data, including whole-brain, hippocampal and basal ganglia volumetry; white matter integrity (diffusion tensor imaging); gray matter density (voxel-based morphometry); and hippocampal microstructural integrity (mean diffusivity and fractional anisotropy). RESULTS: Of the 30 patients included in the study, 19 were male (63%); mean (SD) age was 65.7 (12.3) years. Patients with anti-LGI1 encephalitis had incomplete recovery with significant and persisting verbal (mean [SE] Rey Auditory Verbal Learning Test [RAVLT], delayed recall: patients, 6.52 [1.05]; controls, 11.78 [0.56], P < .001) and visuospatial (Rey-Osterrieth Complex Figure Test [ROCF], delayed recall: patients, 16.0 [1.96]; controls, 25.86 [1.24]; P < .001) memory deficits. These deficits were accompanied by pronounced hippocampal atrophy, including subfields cornu ammonis 2/3 (CA2/3) and CA4/dentate gyrus (DG), as well as impaired hippocampal microstructural integrity. Higher disease severity correlated with larger verbal memory deficits (RAVLT delayed recall, r = −0.40; P = .049), decreased volumes of left hippocampus (r = −0.47; P = .02) and left CA2/3 (r = −0.41; P = .04) and CA4/DG (r = −0.43; P = .03) subfields, and impaired left hippocampal microstructural integrity (r = 0.47; P = .01). In turn, decreased volume of the left CA2/3 subfield (RAVLT delayed recall, r = 0.40; P = .047) and impaired left hippocampal microstructural integrity (RAVLT recognition, r = −0.41; P = .04) correlated with verbal memory deficits. Basal ganglia MRI signal abnormalities were observed in only 1 patient, but a longer duration of faciobrachial dystonic seizures correlated with a reduction of pallidum volume (r = −0.71; P = .03). In contrast, no abnormalities of cortical gray matter or white matter were found. The latency between disease onset and initiation of immunotherapy was significantly correlated with verbal (RAVLT recall after interference, r = −0.48; P = .02) and visuospatial (ROCF delayed recall, r = −0.46; P = .03) memory deficits. CONCLUSIONS AND RELEVANCE: Anti-LGI1 encephalitis is associated with cognitive deficits and disability as a result of structural damage to the hippocampal memory system. This damage might be prevented by early immunotherapy.</abstract><cop>United States</cop><pub>American Medical Association</pub><pmid>27893017</pmid><doi>10.1001/jamaneurol.2016.4226</doi><tpages>10</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Aged Autoantibodies - blood Basal Ganglia - diagnostic imaging Cognition Disorders - etiology Cross-Sectional Studies Disability Evaluation Female HEK293 Cells - metabolism Hippocampus - diagnostic imaging Humans Immunotherapy Intracellular Signaling Peptides and Proteins Limbic Encephalitis - blood Limbic Encephalitis - complications Limbic Encephalitis - diagnostic imaging Limbic Encephalitis - therapy Longitudinal Studies Magnetic Resonance Imaging Male Middle Aged Neuropsychological Tests Proteins - immunology Retrospective Studies |
| title | Evaluation of Cognitive Deficits and Structural Hippocampal Damage in Encephalitis With Leucine-Rich, Glioma-Inactivated 1 Antibodies |
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