Cited by 131Schizophrenia research and treatmentAdvanced MRI Techniques and ApplicationsMental Health and Psychiatry

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Proton Magnetic Resonance Spectroscopy and Illness Stage in Schizophrenia—A Systematic Review and Meta-Analysis

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Brugger, Stefan, Davis, John M., Leucht, Stefan, Stone, James M.·2011·Biological Psychiatry

DOI 10.1016/j.biopsych.2010.10.004

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Abstract

Background It is not known whether regional brain N-acetyl aspartate (NAA) changes in the progression from prodrome to chronic schizophrenia. We used effect size meta-analysis to determine which brain regions show the most robust reductions in NAA first episode and chronic schizophrenia as measured by proton magnetic resonance spectroscopy and to determine whether these changes are present in individuals at high risk of developing schizophrenia. Methods We identified 131 articles, of which 97 met inclusion criteria. Data were separated by stage of illness (at risk, first episode schizophrenia, chronic schizophrenia) and by brain region. For each region, mean and SD of the NAA measure was extracted. Results Significant reductions in NAA levels were found in frontal lobe, temporal lobe, and thalamus in both patient groups (effect size > .3; p < .01). In individuals at high risk of schizophrenia (of whom approximately 20% would be expected to undergo transition to psychosis), significant NAA reductions were present in thalamus (effect size = .78; p < .05), with reductions at trend level only in temporal lobe (effect size = .32; p < .1), and no reductions in frontal lobe (effect size = .05; p = .5). Conclusions These data suggest that schizophrenia is associated with loss of neuronal integrity in frontal and temporal cortices and in the thalamus and suggest that these changes in the frontal and temporal lobe might occur in the transition between the at-risk phase and the first episode.

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BackgroundMethodInfluential
Effects of cannabis and familial loading on subcortical brain volumes in first-episode schizophrenia
Malchow, B., Hasan, A., Schneider-Axmann, T., Jatzko, A., Gruber, O., Schmitt, A., Falkai, P., & Wobrock, T. (2013) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-013-0451-y · Cited by 30
“Meta-analyses from proton magnetic resonance spectroscopy (MRS) studies in FES patients showed reductions in N-acetyl aspartate (NAA) in cortical regions, hippocampus and thalamus, while there seems to be no difference between first-episode and chronic schizophrenia (SZ) patients [11, 69].”
Background
Dysfunctional Cortical Connectivity During the Auditory Oddball Task in Patients with Schizophrenia
Fujimoto, T., Okumura, E., Takeuchi, K., Kodabashi, A., Otsubo, T., Nakamura, K., Kamiya, S., Higashi, Y., Yuji, T., Honda, K., et al. (2013) · The Open Neuroimaging Journal · doi:10.2174/1874440001307010015 · Cited by 28
Reduced GABA/glutamate in the thalamus of individuals at clinical high risk for psychosis
Quiñones, G. M., Mayeli, A., Yushmanov, V. E., Hetherington, H. P., & Ferrarelli, F. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-020-00920-4 · Cited by 28
Adding Sarcosine to Antipsychotic Treatment in Patients with Stable Schizophrenia Changes the Concentrations of Neuronal and Glial Metabolites in the Left Dorsolateral Prefrontal Cortex
Strzelecki, D., Podgórski, M. T., Kałużyńska, O., Stefańczyk, L., Kotlicka‐Antczak, M., Gmitrowicz, A., & Grzelak, P. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms161024475 · Cited by 27
“However, meta-analyses performed by Steen and Brugger [21,22] found that the NAA concentration in the PFC was similar in patients with a first episode of schizophrenia and in the chronic phase of the disease.”
Background
MR spectroscopy in schizophrenia
Port, J. D., & Agarwal, N. (2011) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.22787 · Cited by 25
“Two groups (Steen et al and Brugger et al) (32,33) have attempted systematic reviews and meta-analyses of the schizophrenia MRS literature.”
BackgroundResultInfluential
Reinforcement Learning Performance and Risk for Psychosis in Youth
Waltz, J. A., Demro, C., Schiffman, J. E., Thompson, E., Kline, E. R., Reeves, G. M., Xu, Z., & Gold, J. M. (2015) · The Journal of Nervous and Mental Disease · doi:10.1097/nmd.0000000000000420 · Cited by 26
“…criteria, such as neuropsychological tests (FusarPoli et al., 2012b), blood-based measures (Benros et al., 2012), structural and functional magnetic resonance imaging (Pantelis et al., 2009), electroencephalography (Correll et al., 2010), and molecular imaging techniques (Brugger et al., 2011).”
Background
Substance use and regional gray matter volume in individuals at high risk of psychosis
Stone, J. M., Bhattacharyya, S., Barker, G. J., & McGuire, P. K. (2011) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2011.06.004 · Cited by 25
Self-citation
Magnetic resonance spectroscopy investigations of functionally defined language areas in schizophrenia patients with and without auditory hallucinations
Homan, P., Vermathen, P., van Swam, C., Federspiel, A., Boesch, C., Strik, W. K., Dierks, T., Hubl, D., & Kreis, R. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.03.009 · Cited by 23
“Overall, we found decreased NAA only in Broca's area in our patient population, which is also in contrast to most of the current literature where generally it is found (though more at long echo time, see below) that NAA in schizophrenia is decreased in frontal and temporal regions and in the thalamus (Brugger et al.,…”
Influential
N-Acetylaspartate Reduction in the Medial Prefrontal Cortex Following 8 weeks of Risperidone Treatment in First-Episode Drug-Naïve Schizophrenia Patients
Zong, X., Hu, M., Li, Z., Cao, H., Hé, Y., Liao, Y., Zhou, J., Sang, D., Zhao, H., Tang, J., et al. (2015) · Scientific Reports · doi:10.1038/srep09109 · Cited by 22
N-Acetyl-Aspartate Level is Decreased in the Prefrontal Cortex in Subjects At-Risk for Schizophrenia
Mondino, M., Brunelin, J., & Saoud, M. (2013) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2013.00099 · Cited by 22
“(32), which reported no difference in NAA/Cr level between HRS and healthy controls.”
Background
Biomarkers in Psychosis: An Approach to Early Identification and Individualized Treatment
Mirzakhanian, H., Singh, F., & Cadenhead, K. S. (2013) · Biomarkers in Medicine · doi:10.2217/bmm.13.134 · Cited by 21
Altered Development of the Dorsolateral Prefrontal Cortex in Chromosome 22q11.2 Deletion Syndrome: An In Vivo Proton Spectroscopy Study
Shashi, V., Veerapandiyan, A., Keshavan, M. S., Zapadka, M. E., Schoch, K., Kwapil, T. R., Hooper, S. R., & Stanley, J. A. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.04.023 · Cited by 20
N-Acetylaspartate and N-Acetylaspartylglutamate in Central Nervous System Health and Disease
Moffett, J. R., Ariyannur, P. S., Arun, P., & Namboodiri, A. M. A. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-401688-0.00006-9 · Cited by 21
“Schizophrenia is one neuropsychiatric disorder in particular that has been relatively well studied with regard to reduced NAA levels in specific brain areas (Brugger et al., 2011).”
Background
Magnetic resonance spectroscopy studies in subjects with high risk for psychosis: A meta-analysis and review
Roméo, B., Petillion, A., Martelli, C., & Benyamina, A. (2020) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2020.03.006 · Cited by 19
Neuroprotective Effect of Modified Electroconvulsive Therapy for Schizophrenia
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Ketamine administration induces early and persistent neurochemical imbalance and altered NADPH oxidase in mice
Schiavone, S., Morgese, M. G., Bové, M., Colia, A. L., Maffione, A. B., Tucci, P., Trabace, L., & Cuomo, V. (2019) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2019.109750 · Cited by 19
Cortical glutamate, Glx, and total N-acetylaspartate: potential biomarkers of repetitive transcranial magnetic stimulation treatment response and outcomes in major depression
Gonsalves, M. A., White, T. L., Barredo, J., DeMayo, M. M., DeLuca, E., Harris, A. D., & Carpenter, L. L. (2024) · Translational Psychiatry · doi:10.1038/s41398-023-02715-9 · Cited by 21
Markers of Schizophrenia—A Critical Narrative Update
Galińska-Skok, B., & Waszkiewicz, N. (2022) · Journal of Clinical Medicine · doi:10.3390/jcm11143964 · Cited by 19
“Moreover, meta-analysis of brain chemistry in schizophrenia revealed decreased levels of N-acetyl aspartate (marker of neuronal integrity) levels in the frontal lobe, temporal lobe, and thalamus, in FEP and chronic schizophrenia [50].”
Background
Biomarkers for Psychosis: Are We There Yet? Umbrella Review of 1478 Biomarkers
Fuentes‐Claramonte, P., Estradé, A., Solanes, A., Ramella‐Cravaro, V., García‐León, M. Á., de Diego-Adeliño, J., Molins, C., Fung, E., Valentí, M., Anmella, G., et al. (2024) · Schizophrenia Bulletin Open · doi:10.1093/schizbullopen/sgae018 · Cited by 25
“3 Deterioration in neuronal health might precede illness onset, as suggested by evidence for CHR-P individuals, 95,178 although findings in this group have been inconsistent 179 and better-powered prospective studies are required.”
Background
Social isolation stress and chronic glutathione deficiency have a common effect on the glutamine‐to‐glutamate ratio and myo‐inositol concentration in the mouse frontal cortex
Corcoba, A., Rolf Gruetter, A., Kim, Q., & Duarte, J. M. N. (2017) · Journal of Neurochemistry · doi:10.1111/jnc.14116 · Cited by 18
“Moreover, meta-analyses suggested a decline with age and disease duration in the levels of glutamate and glutamine (Schwerk et al. 2014), as well as N-acetylaspartate (Brugger et al. 2011).”
Background
Do reductions in brain N‐acetylaspartate levels contribute to the etiology of some neuropsychiatric disorders?
Ariyannur, P. S., Arun, P., Barry, E. S., Andrews‐Shigaki, B., Bosomtwi, A., Tang, H., Selwyn, R. G., Grunberg, N. E., Moffett, J. R., & Namboodiri, A. M. A. (2013) · Journal of Neuroscience Research · doi:10.1002/jnr.23234 · Cited by 15
“DOI: 10.1002/jnr.23234 VC 2013 Wiley Periodicals, Inc. systems in a number of neurological and psychiatric disorders and substance-abuse conditions (Tsai and Coyle, 1995; Moffett et al., 2007; Brugger et al., 2011; Maddock and Buonocore, 2012).”
BackgroundInfluential
Magnetic Resonance Spectroscopy for Psychiatry
Port, J. D. (2019) · Neuroimaging Clinics of North America · doi:10.1016/j.nic.2019.09.002 · Cited by 15
Metabolite abnormalities in psychosis risk: A meta-analysis of proton magnetic resonance spectroscopy studies
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An integrative study of the microbiome gut-brain-axis and hippocampal inflammation in psychosis: Persistent effects from mode of birth
Joe, P., Clemente, J. C., Piras, E., Wallach, D. S., Robinson‐Papp, J., Boka, E., Remsen, B., Bonner, M., Kimhy, D., Goetz, D. M., et al. (2021) · Schizophrenia Research · doi:10.1016/j.schres.2021.09.019 · Cited by 14
Modular Functional-Metabolic Coupling Alterations of Frontoparietal Network in Schizophrenia Patients
Xiang, Q., Xu, J., Wang, Y., Chen, T., Wang, J., Zhuo, K., Guo, X., Zeljic, K., Li, W., Sun, Y., et al. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00040 · Cited by 15
“About 5–10% reductions in NAA/Cr in the frontal cortex and hippocampus were found and confirmed by meta-analysis (Steen et al., 2005; Brugger et al., 2011).”
Method
Imaging as Tool to Investigate Psychoses and Antipsychotics
Booij, J., & van Amelsvoort, T. (2012) · Handbook of experimental pharmacology · doi:10.1007/978-3-642-25761-2_12 · Cited by 14
Neuro-imagerie cérébrale des premiers épisodes psychotiques
Jardri, R. (2013) · L Encéphale · doi:10.1016/s0013-7006(13)70102-7 · Cited by 12
Clinical and cognitive correlates of the proton magnetic resonance spectroscopy measures in chronic schizophrenia
Szulc, A., Galińska-Skok, B., Tarasów, E., Konarzewska, B., Waszkiewicz, N., Hykiel, R., & Walecki, J. M. (2012) · Medical Science Monitor · doi:10.12659/msm.882909 · Cited by 12
“The most replicated finding relating to schizophrenia obtained by means of 1H MRS is a lower level of NAA (N-acetylaspartate) in the dorsolateral prefrontal cortex, hippocampal area, temporal cortex and thalamus [1].”
Background
Relationship of auditory electrophysiological responses to magnetic resonance spectroscopy metabolites in Early Phase Psychosis
Bartolomeo, L. A., Wright, A. M., Ma, R. E., Hummer, T. A., Francis, M., Visco, A. C., Mehdiyoun, N. F., Bolbecker, A. R., Hetrick, W. P., Dydak, U., et al. (2019) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2019.05.009 · Cited by 12
“Partial Least Squares Analysis of Association Between MRS Metabolites and Electrophysiological Responses in Pooled EPP and Control Subjects Latent variable 1 2 Singular Values 0.828 0.170 Percent variance 96.0 4.0 MRS Metabolite Level Glx 0.316 0.645 NAA 0.492 −0.681 Cho 0.449 0.266 Cre 0.538 −0.121 Ins 0.408 0.187 El…”
BackgroundResultInfluential
Magnetic resonance imaging and spectroscopy: how useful is it for prediction and prognosis?
Condon, B. R. (2011) · The EPMA Journal · doi:10.1007/s13167-011-0086-x · Cited by 12
“In patients with a high risk of developing schizophrenia significant reductions in the amount of NAA are found in the thalamus [24].”
Background
The impact of endurance training and table soccer on brain metabolites in schizophrenia
Rauchmann, B., Ghaseminejad, F., Keeser, D., Keller-Varady, K., Schneider-Axmann, T., Takahashi, S., Karali, T., Helms, G., Dechent, P., Maurus, I., et al. (2019) · Brain Imaging and Behavior · doi:10.1007/s11682-019-00198-1 · Cited by 11
Long term antipsychotic treatment does not alter metabolite concentrations in rat striatum: An in vivo magnetic resonance spectroscopy study
Lindquist, D. M., Dunn, R. S., & Cecil, K. M. (2011) · Schizophrenia Research · doi:10.1016/j.schres.2011.02.019 · Cited by 10
“N IH -PA Author M anuscript N IH -PA Author M anuscript regions (Brugger et al. 2010; Chang et al. 2007; Steen et al. 2005; Theberge et al. 2004; Theberge et al. 2007).”
Background
Age-dependent effects of (+)-MK801 treatment on glutamate release and metabolism in the rat medial prefrontal cortex
Zou, Y., Zhang, H., Chen, X., Ji, W., Mao, L., & Lei, H. C. (2019) · Neurochemistry International · doi:10.1016/j.neuint.2019.104503 · Cited by 10
The relationship between the alterations in metabolite levels in the dorsolateral prefrontal cortex and clinical symptoms of patients with first-episode schizophrenia: a one year follow-up study
Huang, M., Guo, W., Lu, S., Pan, F., Chen, J., Hu, J., Hu, S., Xu, W., Shang, D., & Xu, Y. (2018) · Oncotarget · doi:10.18632/oncotarget.23983 · Cited by 9
“At the baseline, the NAA/Cr levels in the left DLPFC of patients with drug-naïve FES was significantly lower compared with the control groups, which was consistent with many other researches and the metaanalysis conducted by Marsman et al and Brugger et al [25, 26, 28, 37].”
Result
Advanced imaging in first episode psychosis: a systematic review
Mateos, M., Hacein‐Bey, L., Hanafi, R., Mathys, L., Amad, A., Pruvo, J., & Krystal, S. (2023) · Journal of Neuroradiology · doi:10.1016/j.neurad.2023.04.001 · Cited by 8
Progress in the application of molecular imaging in psychiatric disorders
Tan, J., Zhang, G., Hao, J., Cai, H., Wu, D., Su, Z.-X., Liu, B., & Wu, M. (2023) · Psychoradiology · doi:10.1093/psyrad/kkad020 · Cited by 9
Associations between N-Acetylaspartate and white matter integrity in individuals with schizophrenia and unaffected relatives
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Identification of Developmentally Regulated PCP-Responsive Non-Coding RNA, prt6, in the Rat Thalamus
Takebayashi, H., Yamamoto, N., Umino, A., & Nishikawa, T. (2014) · PLoS ONE · doi:10.1371/journal.pone.0097955 · Cited by 8
An overview of functional, structural and neurochemical imaging studies in individuals with a clinical high risk for psychosis
Egerton, A., Borgwardt, S., Tognin, S., Howes, O. D., McGuire, P. K., & Allen, P. (2011) · Neuropsychiatry · doi:10.2217/npy.11.51 · Cited by 8
N-Acetylaspartate Metabolism Underlays the Structural and Functional Units of the Vertebrate Brain: A Bioenergetic Rationale for Clinical Observations of Changes in the Neuronal Biomarker “NAA” in many Human Brain Disorders
Baslow, M. H., & Burlina, A. P. (2012) · Bioenergetics Open access · doi:10.4172/2167-7662.1000102 · Cited by 8
“Perhaps this is the case in certain psychiatric disorders such as schizophrenia where tNAA is reduced but without clear evidence of any cellular pathology [65].”
Background
Sequential change detection and monitoring of temporal trends in random‐effects meta‐analysis
Dogo, S. H., Clark, A., & Kulinskaya, E. (2016) · Research Synthesis Methods · doi:10.1002/jrsm.1222 · Cited by 6
“Similar temporal changes have been reported in education (Hyde et al., 1990), medicine (Gehr et al., 2006), psychology (Brugger et al., 2011; Twenge et al., 2008; Grabe et al., 2008), to mention but a few.”
Alterations of neurometabolism in the dorsolateral prefrontal cortex and thalamus in transition to psychosis patients change under treatment as usual – A two years follow-up 1H/31P-MR-spectroscopy study
Smesny, S., Berberich, D., Gussew, A., Schönfeld, N., Langbein, K., Walther, M., & Reichenbach, J. R. (2021) · Schizophrenia Research · doi:10.1016/j.schres.2020.11.063 · Cited by 7
Pathophysiology of Schizophrenia
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Ex vivo 1H-MRS brain metabolic profiling in a two-hit model of neurodevelopmental disorders: Prenatal immune activation and peripubertal stress
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In Vivo Brain Magnetic Resonance Spectroscopy: A Measurement of Biomarker Sensitivity to Post-Processing Algorithms
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“While the current approach is effective for diseases with gross metabolic changes, such as brain tumors [7], it is less effective for more subtle metabolic changes that occur in diseases such as schizophrenia [8], autism [9], and concussion [10].”
Background
Magnetic Resonance Spectroscopy (MRS) of the Brain
Fayed, N., & Gonzalez-Toledo, E. (2014) · Elsevier eBooks · doi:10.1016/b978-0-444-53632-7.00318-x · Cited by 5
The Effect of Aripiprazole versus Risperidone on Prefrontal Brain Metabolite Levels and Brain Volume in Psychotic Disorders: An Exploratory Study
Liemburg, E. J., Sibeijn‐Kuiper, A., Knegtering, H., & Aleman, A. (2018) · Neuropsychiatry · doi:10.4172/neuropsychiatry.1000339 · Cited by 5
“Lower levels of glutamate and NAA may be indicative of loss of gray and especially white matter tissue that may occur due to the neurotoxicity [4,7,8].”
BackgroundInfluential

Authors: Brugger, S., Davis, J. M., Leucht, S., & Stone, J. M.
Affiliations: St George's, University of London (GB)
University of Maryland, Baltimore (US)
Technical University of Munich (DE)
King's College London (GB)
Corresponding author: Stone, James M.
ORCID: Brugger, Stefan
Davis, John M.
Leucht, Stefan
Stone, James M.
Venue: Biological Psychiatry
Publisher: Elsevier BV
Published: 2011-03
Volume: 69
Issue: 5
Pages: 495-503
ISSN: 0006-3223 (ISSN-L)
DOI: 10.1016/j.biopsych.2010.10.004
OpenAlex: W1983956215
Cited by: 131
References: 133
Citations by year: 2026: 2 · 2025: 2 · 2024: 4 · 2023: 6 · 2022: 2 · 2021: 4 · 2020: 9 · 2019: 14 · 2018: 6 · 2017: 6 · 2016: 7 · 2015: 14 · 2014: 16 · 2013: 15 · 2012: 17
FWCI: 1.76
Type: journal article
Language: en
Open access: green
kclpure.kcl.ac.uk
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Biological Psychiatry (publishedVersion)
PubMed (publishedVersion)
Research Portal (King's College London) (submittedVersion)
ORCA Online Research @Cardiff (Cardiff University) (submittedVersion)
mediaTUM – the media and publications repository of the Technical University Munich (Technical University Munich) (submittedVersion)
Funders: Eli Lilly
Topics: Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
Social Sciences › Arts and Humanities › Philosophy › Mental Health and Psychiatry
Keywords: schizophrenia, N-acetylaspartate, 1H NMR, disease stage, prodromal schizophrenia, first-episode schizophrenia, chronic schizophrenia, clinical high risk for psychosis, thalamus, frontal lobe, temporal lobe, neuronal integrity, brain metabolites
MeSH terms: Aspartic Acid, Data Interpretation, Statistical, Frontal Lobe, Humans, Magnetic Resonance Spectroscopy, Regression Analysis, Risk, Schizophrenia, Schizophrenic Psychology, Temporal Lobe, Thalamus, Publication Bias, Disease Progression

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