Dopamine and Glutamate in Antipsychotic-Responsive Compared With Antipsychotic-Nonresponsive Psychosis: A Multicenter Positron Emission Tomography and Magnetic Resonance Spectroscopy Study (STRATA)

Abstract The variability in the response to antipsychotic medication in schizophrenia may reflect between-patient differences in neurobiology. Recent cross-sectional neuroimaging studies suggest that a poorer therapeutic response is associated with relatively normal striatal dopamine synthesis capac...

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Published in:	Schizophrenia bulletin Vol. 47; no. 2; pp. 505 - 516
Main Authors:	Egerton, Alice, Murphy, Anna, Donocik, Jacek, Anton, Adriana, Barker, Gareth J, Collier, Tracy, Deakin, Bill, Drake, Richard, Eliasson, Emma, Emsley, Richard, Gregory, Catherine J, Griffiths, Kira, Kapur, Shitij, Kassoumeri, Laura, Knight, Laura, Lambe, Emily J B, Lawrie, Stephen M, Lees, Jane, Lewis, Shôn, Lythgoe, David J, Matthews, Julian, McGuire, Philip, McNamee, Lily, Semple, Scott, Shaw, Alexander D, Singh, Krish D, Stockton-Powdrell, Charlotte, Talbot, Peter S, Veronese, Mattia, Wagner, Ernest, Walters, James T R, Williams, Stephen R, MacCabe, James H, Howes, Oliver D
Format:	Journal Article
Language:	English
Published:	US Oxford University Press 16-03-2021
Subjects:	Adult Antipsychotic Agents - pharmacology Corpus Striatum - diagnostic imaging Corpus Striatum - metabolism Cross-Sectional Studies Dopamine - metabolism Female Glutamic Acid - metabolism Gyrus Cinguli - diagnostic imaging Gyrus Cinguli - metabolism Humans Male Middle Aged Positron-Emission Tomography Proton Magnetic Resonance Spectroscopy Psychotic Disorders - diagnostic imaging Psychotic Disorders - drug therapy Psychotic Disorders - metabolism Regular Schizophrenia - diagnostic imaging Schizophrenia - drug therapy Schizophrenia - metabolism Young Adult 1H-MRS schizophrenia antipsychotic response, treatment resistance PET
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Abstract	Abstract The variability in the response to antipsychotic medication in schizophrenia may reflect between-patient differences in neurobiology. Recent cross-sectional neuroimaging studies suggest that a poorer therapeutic response is associated with relatively normal striatal dopamine synthesis capacity but elevated anterior cingulate cortex (ACC) glutamate levels. We sought to test whether these measures can differentiate patients with psychosis who are antipsychotic responsive from those who are antipsychotic nonresponsive in a multicenter cross-sectional study. 1H-magnetic resonance spectroscopy (1H-MRS) was used to measure glutamate levels (Glucorr) in the ACC and in the right striatum in 92 patients across 4 sites (48 responders [R] and 44 nonresponders [NR]). In 54 patients at 2 sites (25 R and 29 NR), we additionally acquired 3,4-dihydroxy-6-[18F]fluoro-l-phenylalanine (18F-DOPA) positron emission tomography (PET) to index striatal dopamine function (Kicer, min−1). The mean ACC Glucorr was higher in the NR than the R group after adjustment for age and sex (F1,80 = 4.27; P = .04). This was associated with an area under the curve for the group discrimination of 0.59. There were no group differences in striatal dopamine function or striatal Glucorr. The results provide partial further support for a role of ACC glutamate, but not striatal dopamine synthesis, in determining the nature of the response to antipsychotic medication. The low discriminative accuracy might be improved in groups with greater clinical separation or increased in future studies that focus on the antipsychotic response at an earlier stage of the disorder and integrate other candidate predictive biomarkers. Greater harmonization of multicenter PET and 1H-MRS may also improve sensitivity.
AbstractList	The variability in the response to antipsychotic medication in schizophrenia may reflect between-patient differences in neurobiology. Recent cross-sectional neuroimaging studies suggest that a poorer therapeutic response is associated with relatively normal striatal dopamine synthesis capacity but elevated anterior cingulate cortex (ACC) glutamate levels. We sought to test whether these measures can differentiate patients with psychosis who are antipsychotic responsive from those who are antipsychotic nonresponsive in a multicenter cross-sectional study. 1 H-magnetic resonance spectroscopy ( 1 H-MRS) was used to measure glutamate levels (Glu corr ) in the ACC and in the right striatum in 92 patients across 4 sites (48 responders [R] and 44 nonresponders [NR]). In 54 patients at 2 sites (25 R and 29 NR), we additionally acquired 3,4-dihydroxy-6-[18F]fluoro- l -phenylalanine ( 18 F-DOPA) positron emission tomography (PET) to index striatal dopamine function ( K i cer , min −1 ). The mean ACC Glu corr was higher in the NR than the R group after adjustment for age and sex ( F 1,80 = 4.27; P = .04). This was associated with an area under the curve for the group discrimination of 0.59. There were no group differences in striatal dopamine function or striatal Glu corr . The results provide partial further support for a role of ACC glutamate, but not striatal dopamine synthesis, in determining the nature of the response to antipsychotic medication. The low discriminative accuracy might be improved in groups with greater clinical separation or increased in future studies that focus on the antipsychotic response at an earlier stage of the disorder and integrate other candidate predictive biomarkers. Greater harmonization of multicenter PET and 1 H-MRS may also improve sensitivity. The variability in the response to antipsychotic medication in schizophrenia may reflect between-patient differences in neurobiology. Recent cross-sectional neuroimaging studies suggest that a poorer therapeutic response is associated with relatively normal striatal dopamine synthesis capacity but elevated anterior cingulate cortex (ACC) glutamate levels. We sought to test whether these measures can differentiate patients with psychosis who are antipsychotic responsive from those who are antipsychotic nonresponsive in a multicenter cross-sectional study. 1H-magnetic resonance spectroscopy (1H-MRS) was used to measure glutamate levels (Glucorr) in the ACC and in the right striatum in 92 patients across 4 sites (48 responders [R] and 44 nonresponders [NR]). In 54 patients at 2 sites (25 R and 29 NR), we additionally acquired 3,4-dihydroxy-6-[18F]fluoro-l-phenylalanine (18F-DOPA) positron emission tomography (PET) to index striatal dopamine function (Kicer, min−1). The mean ACC Glucorr was higher in the NR than the R group after adjustment for age and sex (F1,80 = 4.27; P = .04). This was associated with an area under the curve for the group discrimination of 0.59. There were no group differences in striatal dopamine function or striatal Glucorr. The results provide partial further support for a role of ACC glutamate, but not striatal dopamine synthesis, in determining the nature of the response to antipsychotic medication. The low discriminative accuracy might be improved in groups with greater clinical separation or increased in future studies that focus on the antipsychotic response at an earlier stage of the disorder and integrate other candidate predictive biomarkers. Greater harmonization of multicenter PET and 1H-MRS may also improve sensitivity. The variability in the response to antipsychotic medication in schizophrenia may reflect between-patient differences in neurobiology. Recent cross-sectional neuroimaging studies suggest that a poorer therapeutic response is associated with relatively normal striatal dopamine synthesis capacity but elevated anterior cingulate cortex (ACC) glutamate levels. We sought to test whether these measures can differentiate patients with psychosis who are antipsychotic responsive from those who are antipsychotic nonresponsive in a multicenter cross-sectional study. 1H-magnetic resonance spectroscopy (1H-MRS) was used to measure glutamate levels (Glucorr) in the ACC and in the right striatum in 92 patients across 4 sites (48 responders [R] and 44 nonresponders [NR]). In 54 patients at 2 sites (25 R and 29 NR), we additionally acquired 3,4-dihydroxy-6-[18F]fluoro-l-phenylalanine (18F-DOPA) positron emission tomography (PET) to index striatal dopamine function (Kicer, min-1). The mean ACC Glucorr was higher in the NR than the R group after adjustment for age and sex (F1,80 = 4.27; P = .04). This was associated with an area under the curve for the group discrimination of 0.59. There were no group differences in striatal dopamine function or striatal Glucorr. The results provide partial further support for a role of ACC glutamate, but not striatal dopamine synthesis, in determining the nature of the response to antipsychotic medication. The low discriminative accuracy might be improved in groups with greater clinical separation or increased in future studies that focus on the antipsychotic response at an earlier stage of the disorder and integrate other candidate predictive biomarkers. Greater harmonization of multicenter PET and 1H-MRS may also improve sensitivity. Abstract The variability in the response to antipsychotic medication in schizophrenia may reflect between-patient differences in neurobiology. Recent cross-sectional neuroimaging studies suggest that a poorer therapeutic response is associated with relatively normal striatal dopamine synthesis capacity but elevated anterior cingulate cortex (ACC) glutamate levels. We sought to test whether these measures can differentiate patients with psychosis who are antipsychotic responsive from those who are antipsychotic nonresponsive in a multicenter cross-sectional study. 1H-magnetic resonance spectroscopy (1H-MRS) was used to measure glutamate levels (Glucorr) in the ACC and in the right striatum in 92 patients across 4 sites (48 responders [R] and 44 nonresponders [NR]). In 54 patients at 2 sites (25 R and 29 NR), we additionally acquired 3,4-dihydroxy-6-[18F]fluoro-l-phenylalanine (18F-DOPA) positron emission tomography (PET) to index striatal dopamine function (Kicer, min−1). The mean ACC Glucorr was higher in the NR than the R group after adjustment for age and sex (F1,80 = 4.27; P = .04). This was associated with an area under the curve for the group discrimination of 0.59. There were no group differences in striatal dopamine function or striatal Glucorr. The results provide partial further support for a role of ACC glutamate, but not striatal dopamine synthesis, in determining the nature of the response to antipsychotic medication. The low discriminative accuracy might be improved in groups with greater clinical separation or increased in future studies that focus on the antipsychotic response at an earlier stage of the disorder and integrate other candidate predictive biomarkers. Greater harmonization of multicenter PET and 1H-MRS may also improve sensitivity.
Author	Lees, Jane Talbot, Peter S Lawrie, Stephen M Veronese, Mattia Collier, Tracy Lambe, Emily J B Semple, Scott Walters, James T R Howes, Oliver D Anton, Adriana Deakin, Bill Griffiths, Kira Williams, Stephen R Murphy, Anna McGuire, Philip Barker, Gareth J Matthews, Julian Donocik, Jacek Kapur, Shitij Knight, Laura Gregory, Catherine J Kassoumeri, Laura Emsley, Richard McNamee, Lily Drake, Richard Shaw, Alexander D Lythgoe, David J Stockton-Powdrell, Charlotte Singh, Krish D Eliasson, Emma MacCabe, James H Egerton, Alice Lewis, Shôn Wagner, Ernest
AuthorAffiliation	14 Psychiatric Imaging Group, MRC London Institute of Medical Sciences, Hammersmith Hospital , London, UK 8 Department of Biostatistics and Health Informatics, Institute of Psychiatry, Psychology & Neuroscience, King’s College London , London, UK 11 Centre for Cardiovascular Science, University of Edinburgh , Edinburgh, UK 7 Division of Psychiatry, University of Edinburgh , Edinburgh, UK 9 Faculty of Medicine, Dentistry and Health Sciences, University of Melbourne , Parkville, Victoria, Australia 5 Department of Neuroimaging, Institute of Psychiatry, Psychology & Neuroscience, King’s College London , London, UK 3 Division of Neuroscience and Experimental Psychology, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester , Manchester, UK 6 Division of Psychology and Mental Health, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester , Manchester, UK 13 Division of Informatics, Imaging and Data Sciences, Univer
AuthorAffiliation_xml	– name: 10 CUBRIC, School of Psychology, College of Biomedical and Life Sciences, Cardiff University , Cardiff, UK – name: 2 NIHR Biomedical Research Centre at South London and Maudsley NHS Foundation Trust , London, UK – name: 9 Faculty of Medicine, Dentistry and Health Sciences, University of Melbourne , Parkville, Victoria, Australia – name: 5 Department of Neuroimaging, Institute of Psychiatry, Psychology & Neuroscience, King’s College London , London, UK – name: 6 Division of Psychology and Mental Health, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester , Manchester, UK – name: 12 MRC Centre for Neuropsychiatric Genetics and Genomics, Division of Psychological Medicine and Clinical Neurosciences, School of Medicine, Cardiff University , Cardiff, UK – name: 4 Academic Unit of Radiology, Medical School, Faculty of Medicine, Dentistry & Health, University of Sheffield , Sheffield, UK – name: 11 Centre for Cardiovascular Science, University of Edinburgh , Edinburgh, UK – name: 8 Department of Biostatistics and Health Informatics, Institute of Psychiatry, Psychology & Neuroscience, King’s College London , London, UK – name: 13 Division of Informatics, Imaging and Data Sciences, University of Manchester , Manchester, UK – name: 14 Psychiatric Imaging Group, MRC London Institute of Medical Sciences, Hammersmith Hospital , London, UK – name: 7 Division of Psychiatry, University of Edinburgh , Edinburgh, UK – name: 1 Department of Psychosis Studies, Institute of Psychiatry, Psychology & Neuroscience, King’s College London , London, UK – name: 3 Division of Neuroscience and Experimental Psychology, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester , Manchester, UK
Author_xml	– sequence: 1 givenname: Alice surname: Egerton fullname: Egerton, Alice email: Alice.Egerton@kcl.ac.uk organization: Department of Psychosis Studies, Institute of Psychiatry, Psychology & Neuroscience, King’s College London, London, UK – sequence: 2 givenname: Anna surname: Murphy fullname: Murphy, Anna organization: Division of Neuroscience and Experimental Psychology, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester, UK – sequence: 3 givenname: Jacek surname: Donocik fullname: Donocik, Jacek organization: Department of Psychosis Studies, Institute of Psychiatry, Psychology & Neuroscience, King’s College London, London, UK – sequence: 4 givenname: Adriana surname: Anton fullname: Anton, Adriana organization: Division of Neuroscience and Experimental Psychology, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester, UK – sequence: 5 givenname: Gareth J surname: Barker fullname: Barker, Gareth J organization: NIHR Biomedical Research Centre at South London and Maudsley NHS Foundation Trust, London, UK – sequence: 6 givenname: Tracy surname: Collier fullname: Collier, Tracy organization: Department of Psychosis Studies, Institute of Psychiatry, Psychology & Neuroscience, King’s College London, London, UK – sequence: 7 givenname: Bill surname: Deakin fullname: Deakin, Bill organization: Division of Neuroscience and Experimental Psychology, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester, UK – sequence: 8 givenname: Richard orcidid: 0000-0003-0220-4835 surname: Drake fullname: Drake, Richard organization: Division of Psychology and Mental Health, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester, UK – sequence: 9 givenname: Emma surname: Eliasson fullname: Eliasson, Emma organization: Division of Psychiatry, University of 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givenname: Scott surname: Semple fullname: Semple, Scott organization: Centre for Cardiovascular Science, University of Edinburgh, Edinburgh, UK – sequence: 25 givenname: Alexander D surname: Shaw fullname: Shaw, Alexander D organization: CUBRIC, School of Psychology, College of Biomedical and Life Sciences, Cardiff University, Cardiff, UK – sequence: 26 givenname: Krish D surname: Singh fullname: Singh, Krish D organization: CUBRIC, School of Psychology, College of Biomedical and Life Sciences, Cardiff University, Cardiff, UK – sequence: 27 givenname: Charlotte surname: Stockton-Powdrell fullname: Stockton-Powdrell, Charlotte organization: Division of Psychology and Mental Health, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester, UK – sequence: 28 givenname: Peter S surname: Talbot fullname: Talbot, Peter S organization: Division of Neuroscience and Experimental Psychology, School of Biological Sciences, Faculty of Biology, 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Psychiatry, Psychology & Neuroscience, King’s College London, London, UK – sequence: 34 givenname: Oliver D surname: Howes fullname: Howes, Oliver D organization: Department of Psychosis Studies, Institute of Psychiatry, Psychology & Neuroscience, King’s College London, London, UK
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Issue	2
Keywords	1H-MRS schizophrenia antipsychotic response, treatment resistance PET
Language	English
License	This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. The Author(s) 2020. Published by Oxford University Press on behalf of the Maryland Psychiatric Research Center.
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 J.H.M. and O.D.H. share senior authorship.
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PublicationTitle	Schizophrenia bulletin
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PublicationYear	2021
Publisher	Oxford University Press
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Snippet	Abstract The variability in the response to antipsychotic medication in schizophrenia may reflect between-patient differences in neurobiology. Recent... The variability in the response to antipsychotic medication in schizophrenia may reflect between-patient differences in neurobiology. Recent cross-sectional...
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SubjectTerms	Adult Antipsychotic Agents - pharmacology Corpus Striatum - diagnostic imaging Corpus Striatum - metabolism Cross-Sectional Studies Dopamine - metabolism Female Glutamic Acid - metabolism Gyrus Cinguli - diagnostic imaging Gyrus Cinguli - metabolism Humans Male Middle Aged Positron-Emission Tomography Proton Magnetic Resonance Spectroscopy Psychotic Disorders - diagnostic imaging Psychotic Disorders - drug therapy Psychotic Disorders - metabolism Regular Schizophrenia - diagnostic imaging Schizophrenia - drug therapy Schizophrenia - metabolism Young Adult
Title	Dopamine and Glutamate in Antipsychotic-Responsive Compared With Antipsychotic-Nonresponsive Psychosis: A Multicenter Positron Emission Tomography and Magnetic Resonance Spectroscopy Study (STRATA)
URI	https://www.ncbi.nlm.nih.gov/pubmed/32910150 https://search.proquest.com/docview/2441611383 https://pubmed.ncbi.nlm.nih.gov/PMC7965076
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