Measurement of brain glutathione with magnetic Resonance spectroscopy in Schizophrenia-Spectrum disorders — A systematic review and Meta-Analysis

Bentsen, 2011, Bimodal distribution of polyunsaturated fatty acids in schizophrenia suggests two endophenotypes of the disorder, Biol. Psychiatry, 70, 97, 10.1016/j.biopsych.2011.02.011 Bošković, 2011, Oxidative stress in schizophrenia, Curr. Neuropharmacol., 9, 301, 10.2174/157015911795596595 Bracken, 2013, T2 relaxation effects on apparent N-acetylaspartate concentration in proton magnetic resonance studies of schizophrenia, Psychiatry Res. Neuroimaging, 213, 142, 10.1016/j.pscychresns.2013.03.005 Brandt, 2016, Age-related changes in anterior cingulate cortex glutamate in schizophrenia: A H-1 MRS Study at 7 Tesla, Schizophr. Res., 172, 101, 10.1016/j.schres.2016.02.017 Cohen, 1999, The problem of units and the circumstance for POMP, Multivar. Behav. Res., 34, 315, 10.1207/S15327906MBR3403_2 Coughlin, 2020, A multimodal approach to studying the relationship between peripheral glutathione, brain glutamate, and cognition in health and in schizophrenia, Mol. Psychiatry. Published Online Da Silva, 2018, Glutathione, the major redox regulator, in the prefrontal cortex of individuals at clinical high risk for psychosis, Int. J. Neuropsychopharmacol., 21, 311, 10.1093/ijnp/pyx094 Das, 2019, Antioxidant defense in schizophrenia and bipolar disorder: a meta-analysis of MRS studies of anterior cingulate glutathione, Prog. Neuropsychopharmacol. Biol. Psychiatry, 91, 94, 10.1016/j.pnpbp.2018.08.006 Dempster, 2020, Early treatment response in first episode psychosis: a 7-T magnetic resonance spectroscopic study of glutathione and glutamate, Mol. Psychiatry, 25, 1640, 10.1038/s41380-020-0704-x Do, 2000, Schizophrenia: glutathione deficit in cerebrospinal fluid and prefrontal cortex in vivo, Eur. J. Neurosci., 12, 3721, 10.1046/j.1460-9568.2000.00229.x Duffy, 2014, Glutathione relates to neuropsychological functioning in mild cognitive impairment, Alzheimer’s & Dementia., 10, 67, 10.1016/j.jalz.2013.01.005 Fisher, 2020, Exercise as a protective mechanism against the negative effects of oxidative stress in first-episode psychosis: a biomarker-led study, Transl. Psychiatry, 10, 1, 10.1038/s41398-020-00927-x Gawryluk, 2011, Decreased levels of glutathione, the major brain antioxidant, in post-mortem prefrontal cortex from patients with psychiatric disorders, Int. J. Neuropsychopharmacol., 14, 123, 10.1017/S1461145710000805 Girgis, 2019, Effects of acute N-acetylcysteine challenge on cortical glutathione and glutamate in schizophrenia: A pilot in vivo proton magnetic resonance spectroscopy study, Psychiatry Res., 275, 78, 10.1016/j.psychres.2019.03.018 Godlewska, 2021, Brain glutamate concentration in men with early psychosis: a magnetic resonance spectroscopy case–control study at 7 T, Translational Psychiatry, 11, 10.1038/s41398-021-01477-6 Gunes, 2017, Oxidative metabolism may be associated with negative symptoms in schizophrenia, Psychiatry and Clinical Psychopharmacology., 27, 54, 10.1080/24750573.2017.1293243 Hafizi, 2018, Interaction between TSPO-a neuroimmune marker- and redox status in clinical high risk for psychosis: a PET-MRS study, Neuropsychopharmacology, 43, 1700, 10.1038/s41386-018-0061-5 Hashimoto, 2019, Recent advances in the early intervention in schizophrenia: future direction from preclinical findings, Curr. Psychiatry Rep., 21, 75, 10.1007/s11920-019-1063-7 Hoch, 2017, When are metabolic ratios superior to absolute quantification? a statistical analysis, NMR Biomed., 30, 10.1002/nbm.3710 Iwata, 2021, Glutathione levels and glutathione-glutamate correlation in patients with treatment-resistant schizophrenia, Schizophr Bull Open., 2(1):sgab006 Jeon, 2021, Progressive changes in glutamate concentration in early stages of schizophrenia: a longitudinal 7-tesla MRS study, Schizophrenia Bulletin Open., 2 Kraguljac, 2012, Neurometabolites in schizophrenia and bipolar disorder - a systematic review and meta-analysis, Psychiatry Res., 203, 111, 10.1016/j.pscychresns.2012.02.003 Kreis, 2015, The trouble with quality filtering based on relative cramér-rao lower bounds, Magn. Reson. Med., 75, 15, 10.1002/mrm.25568 Kumar, 2020, Glutathione and glutamate in schizophrenia: a 7T MRS study, Mol. Psychiatry, 25, 873, 10.1038/s41380-018-0104-7 Lesh T.A., Maddock R.J., Howell A., et al. Extracellular free water and glutathione in first-episode psychosis-a multimodal investigation of an inflammatory model for psychosis. Mol Psychiatry. 2019;((Lesh, Maddock, Howell, Wang, Tanase, Daniel Ragland, Niendam, Carter) Department of Psychiatry, University of California, Davis, United States). doi:10.1038/s41380-019-0428-y. Limongi, 2021, Counteracting Effects of Glutathione on the Glutamate-Driven Excitation/Inhibition Imbalance in First-Episode Schizophrenia A 7T MRS and Dynamic Causal Modeling Study, Antioxidants (Basel, Switzerland), 10 Lin, 2021, Minimum reporting standards for in vivo magnetic resonance spectroscopy (mrsinmrs): experts’ consensus recommendations, NMR Biomed., 34, 10.1002/nbm.4484 MacKinley, 2022, Central oxidative stress and early vocational outcomes in first episode psychosis: a 7-tesla magnetic resonance spectroscopy study of glutathione, Schizophr. Bull., 48, 921, 10.1093/schbul/sbac012 Manna, 2015, Obesity, oxidative stress, adipose tissue dysfunction, and the associated health risks: causes and therapeutic strategies, Metab. Syndr. Relat. Disord., 13, 423, 10.1089/met.2015.0095 Matsuzawa, 2008, Negative correlation between brain glutathione level and negative symptoms in schizophrenia: a 3T 1H-MRS study, PLoS One, 3, e1944, 10.1371/journal.pone.0001944 Merritt, 2021, Association of age, antipsychotic medication, and symptom severity in schizophrenia with proton magnetic resonance spectroscopy brain glutamate level: a mega-analysis of individual participant-level data, JAMA Psychiat., 78, 667, 10.1001/jamapsychiatry.2021.0380 Michels, 2018, Psychiatric risk gene Cacna1c determines mitochondrial resilience against oxidative stress in neurons, Cell Death Dis., 9, 1, 10.1038/s41419-018-0676-9 Mikkelsen T, Hearshen D. CHAPTER 28 - Magnetic Resonance Spectroscopy. In: Newton HB, Jolesz FA, eds. Handbook of Neuro-Oncology NeuroImaging. Academic Press; 2008:257-263. doi:10.1016/B978-012370863-2.50030-0. Murray, 2021, Oxidative stress and the pathophysiology and symptom profile of schizophrenia spectrum disorders, Frontiers Psychiatry, 12 Nezhad, 2017, Quantification of glutathione in the human brain by MR spectroscopy at 3 Tesla: comparison of PRESS and MEGA-PRESS, Magn. Reson. Med., 78, 1257, 10.1002/mrm.26532 Öngür, 2009, Creatine abnormalities in schizophrenia and bipolar disorder, Psychiatry Res. Neuroimaging, 172, 44, 10.1016/j.pscychresns.2008.06.002 Page, 2021, The PRISMA 2020 statement: an updated guideline for reporting systematic reviews, BMJ, 372 Pizzino, 2017, Oxidative stress: harms and benefits for human health, Oxid. Med. Cell. Longev., 2017, e8416763, 10.1155/2017/8416763 R Core Team (2023)._R: A Language and Environment for Statistical Computing_. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Ravanfar, 2022, In vivo 7-Tesla MRI investigation of brain iron and its metabolic correlates in chronic schizophrenia, Schizophrenia., 8, 10.1038/s41537-022-00293-1 Reid, 2019, 7T proton magnetic resonance spectroscopy of the anterior cingulate cortex in first-episode schizophrenia, Schizophr. Bull., 45, 180, 10.1093/schbul/sbx190 Reyes-Madrigal, 2019, Striatal glutathione in first-episode psychosis patients measured in vivo with proton magnetic resonance spectroscopy, Arch. Med. Res., 50, 207, 10.1016/j.arcmed.2019.08.003 Rowland, 2016, Elevated brain lactate in schizophrenia: a 7T magnetic resonance spectroscopy study, Transl. Psychiatry, 6, e967, 10.1038/tp.2016.239 Rowland, 2016, Frontal glutamate and γ-aminobutyric acid levels and their associations with mismatch negativity and digit sequencing task performance in schizophrenia, JAMA Psychiat., 73, 166, 10.1001/jamapsychiatry.2015.2680 Sato, 2014, Pivotal role for ROS activation of p38 MAPK in the control of differentiation and tumor-initiating capacity of glioma-initiating cells, Stem Cell Res., 12, 119, 10.1016/j.scr.2013.09.012 Smucny, 2021, Medial prefrontal cortex glutamate is reduced in schizophrenia and moderated by measurement quality: a meta-analysis of proton magnetic resonance spectroscopy studies, Biol. Psychiatry, 90, 643, 10.1016/j.biopsych.2021.06.008 Solberg, 2019, A five-year follow-up study of antioxidants, oxidative stress and polyunsaturated fatty acids in schizophrenia, Acta Neuropsychiatrica., 31, 202, 10.1017/neu.2019.14 Steullet, 2017, Oxidative stress-driven parvalbumin interneuron impairment as a common mechanism in models of schizophrenia, Mol. Psychiatry, 22, 936, 10.1038/mp.2017.47 Sydnor, 2020, A meta-analysis of ultra-high field glutamate, glutamine, GABA and glutathione 1HMRS in psychosis: implications for studies of psychosis risk, Schizophr. Res., 226, 61, 10.1016/j.schres.2020.06.028 Tal, 2012, The role of gray and white matter segmentation in quantitative proton MR spectroscopic imaging, NMR Biomed., 25, 1392, 10.1002/nbm.2812 Taylor, 2017, Neurometabolic abnormalities in schizophrenia and depression observed with magnetic resonance spectroscopy at 7 T, Bjpsych Open., 3, 6, 10.1192/bjpo.bp.116.003756 Terpstra, 2005, Validation of glutathione quantitation from STEAM spectra against edited H-1 NMR spectroscopy at 4T: application to schizophrenia, MAGMA, 18, 276, 10.1007/s10334-005-0012-0 Upthegrove, 2019, Cytokines, oxidative stress and cellular markers of inflammation in schizophrenia, Neuroinflammation and Schizophrenia, 49 Viechtbauer, 2010, Conducting meta-analyses in R with the metafor Package, J. Stat. Softw., 36, 10.18637/jss.v036.i03 Wang, 2019, Assessing brain metabolism with 7-T proton magnetic resonance spectroscopy in patients with first-episode psychosis, JAMA Psychiat., 76, 314, 10.1001/jamapsychiatry.2018.3637 Wijtenburg, 2014, Reproducibility of phase rotation STEAM at 3T: focus on glutathione, Magn. Reson. Med., 72, 603, 10.1002/mrm.24959 Wijtenburg, 2017, Altered glutamate and regional cerebral blood flow levels in schizophrenia: A 1H-MRS and pCASL study, Neuropsychopharmacol., 42, 562, 10.1038/npp.2016.172 Wilson, 2019, Methodological consensus on clinical proton MRS of the brain: review and recommendations, Magn. Reson. Med., 82, 527, 10.1002/mrm.27742 Wood, 2003, Proton magnetic resonance spectroscopy in first episode psychosis and ultra high-risk individuals, Schizophr. Bull., 29, 831, 10.1093/oxfordjournals.schbul.a007049 Wood, 2009, Medial temporal lobe glutathione concentration in first episode psychosis: A H-1-MRS investigation, Neurobiol. Dis., 33, 354, 10.1016/j.nbd.2008.11.018 Xin, 2016, Genetic polymorphism associated prefrontal glutathione and its coupling with brain glutamate and peripheral redox status in early psychosis, Schizophr. Bull., 42, 1185, 10.1093/schbul/sbw038 Yang, 2023, Meta-analytic evidence of elevated choline, reduced N-acetylaspartate, and normal creatine in schizophrenia and their moderation by measurement quality, echo time, and medication status, NeuroImage: Clinical., 39 Young, 2007, Biomarkers of oxidative stress in schizophrenic and control subjects, Prostaglandins Leukot. Essent. Fat. Acids, 76, 73, 10.1016/j.plefa.2006.11.003 Zhang, 2007, Nicotine dependence, symptoms and oxidative stress in male patients with schizophrenia, Neuropsychopharmacol., 32, 2020, 10.1038/sj.npp.1301317