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Clinical, cognitive and neuroanatomical associations of serum NMDAR autoantibodies in people at clinical high risk for psychosis

Clinical, cognitive and neuroanatomical associations of serum NMDAR autoantibodies in people at clinical high risk for psychosis
Clinical, cognitive and neuroanatomical associations of serum NMDAR autoantibodies in people at clinical high risk for psychosis

Serum neuronal autoantibodies, such as those to the NMDA receptor (NMDAR), are detectable in a subgroup of patients with psychotic disorders. It is not known if they are present before the onset of psychosis or whether they are associated with particular clinical features or outcomes. In a case–control study, sera from 254 subjects at clinical high risk (CHR) for psychosis and 116 healthy volunteers were tested for antibodies against multiple neuronal antigens implicated in CNS autoimmune disorders, using fixed and live cell-based assays (CBAs). Within the CHR group, the relationship between NMDAR antibodies and symptoms, cognitive function and clinical outcomes over 24 month follow-up was examined. CHR subjects were not more frequently seropositive for neuronal autoantibodies than controls (8.3% vs. 5.2%; OR = 1.50; 95% CI: 0.58–3.90). The NMDAR was the most common target antigen and NMDAR IgGs were more sensitively detected with live versus fixed CBAs (p < 0.001). Preliminary phenotypic analyses revealed that within the CHR sample, the NMDAR antibody seropositive subjects had higher levels of current depression, performed worse on the Rey Auditory Verbal Learning Task (p < 0.05), and had a markedly lower IQ (p < 0.01). NMDAR IgGs were not more frequent in subjects who later became psychotic than those who did not. NMDAR antibody serostatus and titre was associated with poorer levels of functioning at follow-up (p < 0.05) and the presence of a neuronal autoantibody was associated with larger amygdala volumes (p < 0.05). Altogether, these findings demonstrate that NMDAR autoantibodies are detectable in a subgroup of CHR subjects at equal rates to controls. In the CHR group, they are associated with affective psychopathology, impairments in verbal memory, and overall cognitive function: these findings are qualitatively and individually similar to core features of autoimmune encephalitis and/or animal models of NMDAR antibody-mediated CNS disease. Overall the current work supports further evaluation of NMDAR autoantibodies as a possible prognostic biomarker and aetiological factor in a subset of people already meeting CHR criteria.

1359-4184
1-15
Pollak, Thomas
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Kempton, Matthew
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Iyegbe, Conrad
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Vincent, Angela
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Irani, Sarosh
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Coutinho, Ester
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Menassa, David A
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Jacobson, Leslie
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De Haan, Lieuwe
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Ruhrmann, Stephan
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Sachs, Gabriele
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Riecher-Rössler, Anita
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Nelson, Barnaby
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Rutten, Bart
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Van Os, Jim
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Bressan, Rodrigo
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Hotopf, Matthew
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Valmaggia, Lucia
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Stone, James
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David, Anthony S.
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McGuire, Philip
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van der Gaag, Mark
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Yolken, Robert
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Amminger, G. Paul
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Pollak, Thomas
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Kempton, Matthew
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Iyegbe, Conrad
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Vincent, Angela
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Irani, Sarosh
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Coutinho, Ester
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Menassa, David A
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Jacobson, Leslie
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De Haan, Lieuwe
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Ruhrmann, Stephan
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Sachs, Gabriele
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Riecher-Rössler, Anita
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Krebs, Marie-Odile
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Nelson, Barnaby
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Glenthoej, Birte
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Barrantes-Vidal, Neus
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Rutten, Bart
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Van Os, Jim
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Bressan, Rodrigo
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Hotopf, Matthew
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Valmaggia, Lucia
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Stone, James
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David, Anthony S.
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McGuire, Philip
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van der Gaag, Mark
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Yolken, Robert
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Amminger, G. Paul
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Pollak, Thomas, Kempton, Matthew, Iyegbe, Conrad, Vincent, Angela, Irani, Sarosh, Coutinho, Ester, Menassa, David A, Jacobson, Leslie, De Haan, Lieuwe, Ruhrmann, Stephan, Sachs, Gabriele, Riecher-Rössler, Anita, Krebs, Marie-Odile, Nelson, Barnaby, Glenthoej, Birte, Barrantes-Vidal, Neus, Rutten, Bart, Van Os, Jim, Bressan, Rodrigo, Hotopf, Matthew, Valmaggia, Lucia, Stone, James, David, Anthony S., McGuire, Philip, van der Gaag, Mark, Yolken, Robert and Amminger, G. Paul (2020) Clinical, cognitive and neuroanatomical associations of serum NMDAR autoantibodies in people at clinical high risk for psychosis. Molecular Psychiatry, 1-15. (doi:10.1038/s41380-020-00899-w).

Record type: Article

Abstract

Serum neuronal autoantibodies, such as those to the NMDA receptor (NMDAR), are detectable in a subgroup of patients with psychotic disorders. It is not known if they are present before the onset of psychosis or whether they are associated with particular clinical features or outcomes. In a case–control study, sera from 254 subjects at clinical high risk (CHR) for psychosis and 116 healthy volunteers were tested for antibodies against multiple neuronal antigens implicated in CNS autoimmune disorders, using fixed and live cell-based assays (CBAs). Within the CHR group, the relationship between NMDAR antibodies and symptoms, cognitive function and clinical outcomes over 24 month follow-up was examined. CHR subjects were not more frequently seropositive for neuronal autoantibodies than controls (8.3% vs. 5.2%; OR = 1.50; 95% CI: 0.58–3.90). The NMDAR was the most common target antigen and NMDAR IgGs were more sensitively detected with live versus fixed CBAs (p < 0.001). Preliminary phenotypic analyses revealed that within the CHR sample, the NMDAR antibody seropositive subjects had higher levels of current depression, performed worse on the Rey Auditory Verbal Learning Task (p < 0.05), and had a markedly lower IQ (p < 0.01). NMDAR IgGs were not more frequent in subjects who later became psychotic than those who did not. NMDAR antibody serostatus and titre was associated with poorer levels of functioning at follow-up (p < 0.05) and the presence of a neuronal autoantibody was associated with larger amygdala volumes (p < 0.05). Altogether, these findings demonstrate that NMDAR autoantibodies are detectable in a subgroup of CHR subjects at equal rates to controls. In the CHR group, they are associated with affective psychopathology, impairments in verbal memory, and overall cognitive function: these findings are qualitatively and individually similar to core features of autoimmune encephalitis and/or animal models of NMDAR antibody-mediated CNS disease. Overall the current work supports further evaluation of NMDAR autoantibodies as a possible prognostic biomarker and aetiological factor in a subset of people already meeting CHR criteria.

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Accepted/In Press date: 21 September 2020
e-pub ahead of print date: 19 October 2020

Identifiers

Local EPrints ID: 444462
URI: http://eprints.soton.ac.uk/id/eprint/444462
ISSN: 1359-4184
PURE UUID: 4b7e6858-189e-4e18-b2e6-83e3e3f9d2c9

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Date deposited: 20 Oct 2020 16:31
Last modified: 16 Mar 2024 09:25

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Contributors

Author: Thomas Pollak
Author: Matthew Kempton
Author: Conrad Iyegbe
Author: Angela Vincent
Author: Sarosh Irani
Author: Ester Coutinho
Author: David A Menassa
Author: Leslie Jacobson
Author: Lieuwe De Haan
Author: Stephan Ruhrmann
Author: Gabriele Sachs
Author: Anita Riecher-Rössler
Author: Marie-Odile Krebs
Author: Barnaby Nelson
Author: Birte Glenthoej
Author: Neus Barrantes-Vidal
Author: Bart Rutten
Author: Jim Van Os
Author: Rodrigo Bressan
Author: Matthew Hotopf
Author: Lucia Valmaggia
Author: James Stone
Author: Anthony S. David
Author: Philip McGuire
Author: Mark van der Gaag
Author: Robert Yolken
Author: G. Paul Amminger

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