Measurement of brain metabolites by 1H magnetic resonance spectroscopy in patients with schizophrenia: a systematic review and meta-analysis

Steen, R Grant; Hamer, Robert M; Lieberman, Jeffrey A

doi:10.1038/sj.npp.1300850

Cited by 254Schizophrenia research and treatmentAdvanced MRI Techniques and ApplicationsMental Health and Psychiatry

Measurement of brain metabolites by 1H magnetic resonance spectroscopy in patients with schizophrenia: a systematic review and meta-analysis

Steen, R Grant, Hamer, Robert M, Lieberman, Jeffrey A·2005·Neuropsychopharmacology

DOI 10.1038/sj.npp.1300850

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Abstract

A systematic review of the literature identified 64 published English-language papers that used proton (1H) magnetic resonance spectroscopy to measure N-acetylaspartate (NAA) concurrently in healthy controls and in patients with a diagnosis of schizophrenia (SZ). A total of 1209 controls and 1256 patients have been evaluated, with 88% of studies carried out at 1.5 T field strength, and 77% of studies focused on patients with chronic SZ. There is consistent evidence that NAA is reduced in a broad range of tissues in the SZ brain. Broad consensus (> or =10 studies) is emerging that NAA levels are reduced > or =5% in hippocampus and in both cortical gray matter (GM) and white matter (WM) of the frontal lobe. There is no evidence to support a hypothesis that relative NAA levels are reduced to a different degree in frontal lobe GM and WM, nor is there robust evidence of a difference in NAA levels between patients with first-episode and chronic SZ. Study reliability may be a problem, as most studies appear to be underpowered. With simple assumptions about the inherent difference in NAA levels between patients and controls, it can be calculated that a minimum sample size of approximately 39 patients and 39 controls is required for acceptable statistical power. Only three of 64 studies included enough subjects to have 80% power to detect a 10% NAA reduction in patients, and no studies were adequately powered to detect a 5% NAA reduction with 80% power.

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An earlier meta-analysis made clear that N-acetyl aspartate levels are reduced in patients with schizophrenia in frontal lobe gray and white matter.
“An earlier meta-analysis made clear that N-acetyl aspartate levels are reduced in patients with schizophrenia in frontal lobe gray and white matter.60”
From Glutamate in Schizophrenia: A Focused Review and Meta-Analysis of 1H-MRS Studies (2013) · cites this paper as [60]

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Deicken, R. F., Johnson, C., Eliaz, Y., & Schuff, N. W. (2000) · American Journal of Psychiatry · doi:10.1176/appi.ajp.157.4.644 · Cited by 57 · see citing works
Lower Concentration of Thalamic N-Acetylaspartate in Patients With Schizophrenia: A Replication Study
Ende, G., Braus, D. F., Walter, S., & Henn, F. A. (2001) · American Journal of Psychiatry · doi:10.1176/appi.ajp.158.8.1314 · Cited by 57 · see citing works
Proton magnetic resonance spectroscopy of basal ganglia in chronic schizophrenia
Fujimoto, T., Nakano, T., Takano, T., Takeuchi, K., Yamada, K., Fukuzako, T., & Akimoto, H. (1996) · Biological Psychiatry · doi:10.1016/0006-3223(95)00316-9 · Cited by 56 · see citing works
Proton magnetic resonance spectroscopy in schizophrenia
Bertolino, A., & Weinberger, D. R. (1999) · European Journal of Radiology · doi:10.1016/s0720-048x(99)00052-2 · Cited by 54 · see citing works
Thalamic abnormalities in patients with schizophrenia revealed by proton magnetic resonance spectroscopy
Omori, M., Murata, T., Kimura, H., Koshimoto, Y., Kado, H., Ishimori, Y., Ito, H., & Wada, Y. (2000) · Psychiatry Research Neuroimaging · doi:10.1016/s0925-4927(00)00049-4 · Cited by 53 · see citing works
Proton Magnetic Resonance Spectroscopy of the Medial Prefrontal Cortex in Patients With Deficit Schizophrenia: Preliminary Report
Delamillieure, P., Fernandez, J. Μ., Constans, J., Brazo, P., Benali, K., Abadie, P., Vasse, T., Thibaut, F., Courthè®μx, P., Petit, M., et al. (2000) · American Journal of Psychiatry · doi:10.1176/appi.ajp.157.4.641 · Cited by 52 · see citing works
Neuropsychological Correlates of Basal Ganglia and Medial Temporal Lobe NAA/Cho Reductions in Traumatic Brain Injury
Ariza, M., Junqué, C., Mataró, M., Poca, M. A., Bargalló, N., Olondo, M., & Sahuquillo, J. (2004) · Archives of Neurology · doi:10.1001/archneur.61.4.541 · Cited by 51 · see citing works
Frontal lobe of children with schizophrenia spectrum disorders: A proton magnetic resonance spectroscopic study
Brooks, W. M., Hodde-Vargas, J., Vargas, A., Yeo, R. A., Ford, C. C., & Hendren, R. L. (1998) · Biological Psychiatry · doi:10.1016/s0006-3223(97)00462-9 · Cited by 49 · see citing works
Reproducibility of 1H‐MRS measurements in schizophrenic patients
Mullins, P. G., Rowland, L. M., Bustillo, J., Bedrick, E. J., Lauriello, J., & Brooks, W. M. (2003) · Magnetic Resonance in Medicine · doi:10.1002/mrm.10598 · Cited by 47 · see citing works
In vitro 1H-magnetic resonance spectroscopy of postmortem brains with schizophrenia
Omori, M., Pearce, J., Komoroski, R. A., Griffin, W. S. T., Mrak, R. E., Husain, M. M., & Karson, C. N. (1997) · Biological Psychiatry · doi:10.1016/s0006-3223(96)00409-x · Cited by 46 · see citing works
Evidence of Neuronal Injury Outside the Medial Temporal Lobe in Temporal Lobe Epilepsy:N-Acetylaspartate Concentration Reductions Detected with Multisection Proton MR Spectroscopic Imaging—Initial Experience
Vermathen, P., Laxer, K. D., Schuff, N. W., Matson, G. B., & Weiner, M. W. (2003) · Radiology · doi:10.1148/radiol.2261011668 · Cited by 46 · see citing works
The value of proton MR spectroscopy in pediatric metabolic brain disease.
Zimmerman, R. A., & Wang, Z. (1998) · PubMed · Cited by 46 · see citing works
1H MRSI evidence of metabolic abnormalities in childhood-onset schizophrenia
O’Neill, J., Levitt, J. G., Caplan, R., Asarnow, R., McCracken, J. T., Toga, A. W., & Alger, J. R. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2003.11.005 · Cited by 45 · see citing works
Evidence for altered cerebellar vermis neuronal integrity in schizophrenia
Deicken, R. F., Feiwell, R., Schuff, N. W., & Soher, B. J. (2001) · Psychiatry Research Neuroimaging · doi:10.1016/s0925-4927(01)00103-2 · Cited by 44 · see citing works
Proton magnetic resonance spectroscopy of the basal ganglia in patients with schizophrenia: a preliminary report
Shioiri, T., Hamakaw, H., Kato, T., Murashita, J., Fujii, K., Inubushi, T., & Takahashi, S. (1996) · Schizophrenia Research · doi:10.1016/0920-9964(96)00017-5 · Cited by 44 · see citing works
Hippocampal age-related changes in schizophrenia: a proton magnetic resonance spectroscopy study
Maier, M., & Ron, M. A. (1996) · Schizophrenia Research · doi:10.1016/0920-9964(96)00044-8 · Cited by 43 · see citing works
Multiregional 1 H-MRSI of the hippocampus, thalamus, and basal ganglia in schizophrenia
Ende, G., Braus, D. F., Walter, S., Weber‐Fahr, W., & Henn, F. A. (2003) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-003-0398-5 · Cited by 34 · see citing works
Proton magnetic resonance spectroscopy of the inferior frontal gyrus and thalamus and its relationship to verbal learning task performance in patients with schizophrenia: A preliminary report
Hagino, H., Suzuki, M., Mori, K., Nohara, S., Yamashita, I., Takahashi, T., Kurokawa, K., Matsui, M., Watanabe, N., Seto, H., et al. (2002) · Psychiatry and Clinical Neurosciences · doi:10.1046/j.1440-1819.2002.01045.x · Cited by 34 · see citing works
PROTON MR SPECTROSCOPY OF PEDIATRIC BRAIN TUMORS
Taylor, J. S., Ogg, R. J., & Langston, J. W. (1998) · Neuroimaging Clinics of North America · doi:10.1016/s1052-5149(25)00539-8 · Cited by 32 · see citing works
Basal ganglia N-acetylaspartate correlates with the performance in the procedural task ‘Tower of Hanoi’ of neuroleptic-naive schizophrenic patients
Giménez, M., Junqué, C., Pérez, M., Vendrell, P., Baeza, I., Salamero, M., Mercader, J. M., & Bernardo, M. (2003) · Neuroscience Letters · doi:10.1016/s0304-3940(03)00698-0 · Cited by 32 · see citing works
Subtype-associated metabolite differences in the temporal lobe in schizophrenia detected by proton magnetic resonance spectroscopy
Fukuzako, H., Kodama, S., Fukuzako, T., Yamada, K., Doi, W., Sato, D., & Takigawa, M. (1999) · Psychiatry Research Neuroimaging · doi:10.1016/s0925-4927(99)00035-9 · Cited by 31 · see citing works
Single-voxel proton magnetic resonance spectroscopy of the pons and cerebellum in patients with schizophrenia: a preliminary study1A portion of this investigation was presented at the Biennial Meeting of International Congress on Schizophrenia Research, Colorado Springs, CO, April 13, 1997.1
Eluri, R., Paul, C. R., Roemer, R., & Boyko, O. B. (1998) · Psychiatry Research Neuroimaging · doi:10.1016/s0925-4927(98)00043-2 · Cited by 30 · see citing works
Correlation of Basal Ganglia Magnetic Resonance Spectroscopy With Apgar Score in Perinatal Asphyxia
Pavlakis, S. G., Kingsley, P. B., Harper, R., Buckwald, S., Spinazzola, R., Frank, Y., & Prohovnik, I. (1999) · Archives of Neurology · doi:10.1001/archneur.56.12.1476 · Cited by 25 · see citing works
Abnormally high levels of brain N-acetylaspartate in children with sickle cell disease.
Steen, R. G., & Ogg, R. J. (2005) · PubMed · Cited by 24 · see citing works
Neural damage in the lenticular nucleus linked with tardive dyskinesia in schizophrenia: a preliminary study using proton magnetic resonance spectroscopy
Ando, K., Takei, N., Matsumoto, H., Iyo, M., Isoda, H., & Mori, N. (2002) · Schizophrenia Research · doi:10.1016/s0920-9964(01)00290-0 · Cited by 21 · see citing works
Proton magnetic resonance spectroscopy of lenticular nuclei in simple schizophrenia
Ohara, K., Isoda, H., Suzuki, Y., Takehara, Y., Ochiai, M., Takeda, H., Hattori, K., Igarashi, Y., & Ohara, K. (2000) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/s0278-5846(00)00089-0 · Cited by 20 · see citing works
Proton MR spectroscopy of Wernicke encephalopathy.
Mascalchi, M., Belli, G., Guerrini, L., Nistri, M., Seppia, I. D., & Villari, N. (2002) · PubMed Central · Cited by 20 · see citing works
Heritability Heightens Brain Metabolite Differences in Schizophrenia
Fukuzako, H. (2000) · Journal of Neuropsychiatry · doi:10.1176/jnp.12.1.95 · Cited by 18 · see citing works
Proton magnetic resonance spectroscopy (1H-MRS) of the cerebellum in men with schizophrenia.
Tibbo, P. G., Hanstock, C. C., Asghar, S., Silverstone, P. H., & Allen, P. S. (2000) · PubMed Central · Cited by 17 · see citing works
Proton magnetic resonance spectroscopy in children with Moyamoya disease
Shimizu, H., Shirane, R., Fujiwara, S., Takahashi, A., & Yoshimoto, T. (1997) · Clinical Neurology and Neurosurgery · doi:10.1016/s0303-8467(97)00059-0 · Cited by 15 · see citing works
Differences in fMRI and MRS in a monozygotic twin pair discordant for schizophrenia (case report)
Španiel, F., Hájek, T., Tintěra, J., Harantová, P., Dezortová, M., & Hájek, M. (2003) · Acta Psychiatrica Scandinavica · doi:10.1034/j.1600-0447.2003.02430.x · Cited by 13 · see citing works
Brain metabolite concentration ratios in vivo: multisite reproducibility by single-voxel 1H MR spectroscopy
Komoroski, R. A., Kotrla, K. J., Lemen, L. C., Lindquist, D. M., Diaz, P., & Foundas, A. L. (2004) · Magnetic Resonance Imaging · doi:10.1016/j.mri.2003.12.001 · Cited by 12 · see citing works
Mesial temporal lobe Cho to Cr(PCr) ratio asymmetry in chronic schizophrenics
Moore, C. M., Bonello, C. M., Sherwood, A. R., Cohen, B. M., Renshaw, P. F., & Yurgelun-Todd, D. A. (2002) · Schizophrenia Research · doi:10.1016/s0920-9964(01)00302-4 · Cited by 10 · see citing works

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N-Acetylaspartate in the CNS: From neurodiagnostics to neurobiology
MOFFETT, J., Ross, B., Arun, P., Madhavarao, C. N., & Namboodiri, A. M. (2007) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2006.12.003 · Cited by 1,407 · see citing works
Cognitive Control Deficits in Schizophrenia: Mechanisms and Meaning
Lesh, T. A., Niendam, T. A., Minzenberg, M., & Carter, C. S. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.156 · Cited by 495 · see citing works
Glutamate in Schizophrenia: A Focused Review and Meta-Analysis of 1H-MRS Studies
Marsman, A., van den Heuvel, M. P., Klomp, D. W. J., Kahn, R. S., Luijten, P. R., & Hulshoff Pol, H. E. (2013) · Schizophrenia Bulletin · doi:10.1093/schbul/sbr069 · Cited by 457 · see citing works
Disrupted-in-Schizophrenia 1 (DISC1) regulates spines of the glutamate synapse via Rac1
Hayashi-Takagi, A., Takaki, M., Graziane, N., Seshadri, S., Murdoch, H., Dunlop, A. J., Makino, Y., Seshadri, A. J., Ishizuka, K., Srivastava, D. P., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2487 · Cited by 399 · see citing works
Schizophrenia, “Just the Facts”: What we know in 2008
Tandon, R., Keshavan, M. S., & Nasrallah, H. A. (2008) · Schizophrenia Research · doi:10.1016/j.schres.2008.01.022 · Cited by 412 · see citing works
The Consortium on the Genetics of Schizophrenia: Neurocognitive Endophenotypes
Gur, R. C., Calkins, M. E., Gur, R. C., Horan, W. P., Nuechterlein, K. H., Seidman, L. J., & Stone, W. S. (2006) · Schizophrenia Bulletin · doi:10.1093/schbul/sbl055 · Cited by 383 · see citing works
Schizophrenia, “just the facts”: What we know in 2008Part 3: Neurobiology
Keshavan, M. S., TANDON, R., Boutros, N. N., & Nasrallah, H. A. (2008) · Schizophrenia Research · doi:10.1016/j.schres.2008.07.020 · Cited by 345 · see citing works
Mitochondrial involvement in psychiatric disorders
Shao, L., Martin, M. V., Watson, S. J., Schatzberg, A. F., Akil, H., Myers, R., Jones, E. G., Bunney, W. E., & Vawter, M. P. (2008) · Annals of Medicine · doi:10.1080/07853890801923753 · Cited by 303 · see citing works
Elevated prefrontal cortex γ-aminobutyric acid and glutamate-glutamine levels in schizophrenia measured in vivo with proton magnetic resonance spectroscopy
Mao, X. (2012) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2011.1519 · Cited by 296 · see citing works
Metabolic Profiling of CSF: Evidence That Early Intervention May Impact on Disease Progression and Outcome in Schizophrenia
Holmes, E. C., Tsang, T. M., Huang, J. T.-J., Leweke, F. M., Koethe, D., Gerth, C. W., Nolden, B. M., Gross, S., Schreiber, D., Nicholson, J. K., et al. (2006) · PLoS Medicine · doi:10.1371/journal.pmed.0030327 · Cited by 292 · see citing works
Neurofunctional correlates of vulnerability to psychosis: A systematic review and meta-analysis
Fusar‐Poli, P., Pérez, J., Broome, M. R., Borgwardt, S., Placentino, A., Caverzasi, E., Cortesi, M., Veggiotti, P., Politi, P., Barale, F., et al. (2007) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2006.11.006 · Cited by 290 · see citing works
MR Spectroscopic Studies of the Brain in Psychiatric Disorders
Maddock, R. J., & Buonocore, M. H. (2011) · Current topics in behavioral neurosciences · doi:10.1007/7854_2011_197 · Cited by 266 · see citing works
Response variability in Attention-Deficit/Hyperactivity Disorder: a neuronal and glial energetics hypothesis.
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Higher Levels of Glutamate in the Associative-Striatum of Subjects with Prodromal Symptoms of Schizophrenia and Patients with First-Episode Psychosis
de la Fuente-Sandoval, C., León-Ortíz, P., Favila, R., Stephano, S., Mamo, D., Ramírez-Bermúdez, J., & Graff-Guerrero, A. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.65 · Cited by 248 · see citing works
Mitochondrial Variants in Schizophrenia, Bipolar Disorder, and Major Depressive Disorder
Rollins, B. L., Martin, M. V., Sequeira, A., Moon, E. A., Morgan, L. Z., Watson, S. J., Schatzberg, A. F., Akil, H., Myers, R., Jones, E. G., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004913 · Cited by 212 · see citing works
Neurometabolites in schizophrenia and bipolar disorder — A systematic review and meta-analysis
Kraguljac, N. V., Reid, M. A., White, D. M., Jones, R., den Hollander, J., Lowman, D., & Lahti, A. C. (2012) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2012.02.003 · Cited by 204 · see citing works
Increased Hippocampal Glutamate and Volumetric Deficits in Unmedicated Patients With Schizophrenia
Kraguljac, N. V., White, D. M., Reid, M. A., & Lahti, A. C. (2013) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2013.2437 · Cited by 191 · see citing works
Longitudinal grey-matter and glutamatergic losses in first-episode schizophrenia
Théberge, J., Williamson, K. E., Aoyama, N., Drost, D. J., Manchanda, R., Malla, A. K., Northcott, S., Menon, R. S., Neufeld, R. W. J., Rajakumar, N., et al. (2007) · British Journal of Psychiatry · doi:10.1192/bjp.bp.106.033670 · Cited by 185 · see citing works
The schizophrenia syndrome, circa 2024: What we know and how that informs its nature
Tandon, R., Nasrallah, H. A., Akbarian, S., Carpenter, W. T., DeLisi, L. E., Gäebel, W., Green, M. F., Gur, R. E., Heckers, S., Kane, J. M., et al. (2023) · Schizophrenia Research · doi:10.1016/j.schres.2023.11.015 · Cited by 196 · see citing works
Glutamate Levels in the Associative Striatum Before and After 4 Weeks of Antipsychotic Treatment in First-Episode Psychosis
de la Fuente‐Sandoval, C., León-Ortíz, P., Azcárraga, M., Stephano, S., Favila, R., Díaz-Galvis, L., Alvarado-Alanis, P., Ramírez‐Bermúdez, J., & Graff‐Guerrero, A. (2013) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2013.289 · Cited by 181 · see citing works
Assessing Brain Metabolism With 7-T Proton Magnetic Resonance Spectroscopy in Patients With First-Episode Psychosis
Wang, A. M., Pradhan, S., Coughlin, J. M., Trivedi, A. M., DuBois, S. L., Crawford, J. L., Sedlak, T. W., Nucifora, F. C., Nestadt, G., Nucifora, L. G., et al. (2019) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2018.3637 · Cited by 158 · see citing works
Deconstructing Psychosis With Human Brain Imaging
Gur, R. C., Keshavan, M. S., & Lawrie, S. M. (2007) · Schizophrenia Bulletin · doi:10.1093/schbul/sbm045 · Cited by 160 · see citing works
1H-MRS at 4 Tesla in minimally treated early schizophrenia
Bustillo, J. R., Rowland, L. M., Mullins, P., Jung, R., Chen, H., Qualls, C., Hammond, R., Brooks, W. M., & Lauriello, J. (2010) · Molecular Psychiatry · doi:10.1038/mp.2009.121 · Cited by 153 · see citing works
Brain GABA and glutamate levels across pain conditions: A systematic literature review and meta-analysis of 1H-MRS studies using the MRS-Q quality assessment tool
Peek, A. L., Rebbeck, T. J., Puts, N. A. J., Watson, J., Aguila, M. E. R., & Leaver, A. M. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.116532 · Cited by 152 · see citing works
GABA and glutamate in schizophrenia: A 7 T 1H-MRS study
Marsman, A., Mandl, R. C. W., Klomp, D. W. J., Bohlken, M. M., Boer, V. O., Андрейченко, А. Е., Cahn, W., Kahn, R. S., Luijten, P. R., & Pol, H. E. H. (2014) · NeuroImage Clinical · doi:10.1016/j.nicl.2014.10.005 · Cited by 150 · see citing works
Glutamate-mediated excitotoxicity in schizophrenia: a review.
Plitman, E., Nakajima, S., de la Fuente-Sandoval, C., Gerretsen, P., Chakravarty, M., Kobylianskii, J., Chung, J., Caravaggio, F., Iwata, Y., Remington, G., et al. (2014) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2014.07.015 · Cited by 151 · see citing works
Baseline effects of transcranial direct current stimulation on glutamatergic neurotransmission and large-scale network connectivity
Hunter, M. A., Coffman, B. A., Gasparovic, C., Calhoun, V. D., Trumbo, M., & Clark, V. P. (2014) · Brain Research · doi:10.1016/j.brainres.2014.09.066 · Cited by 132 · see citing works
Proton Magnetic Resonance Spectroscopy and Illness Stage in Schizophrenia—A Systematic Review and Meta-Analysis
Brugger, S., Davis, J. M., Leucht, S., & Stone, J. M. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.10.004 · Cited by 131 · see citing works
Neuropathological, neurogenetic and neuroimaging evidence for white matter pathology in schizophrenia
Walterfang, M., Wood, S. J., Velakoulis, D., & Pantelis, C. (2006) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2006.02.001 · Cited by 131 · see citing works
Proton MRS in twin pairs discordant for schizophrenia
Lutkenhoff, E. S., van Erp, T. G., Thomas, M. A., Therman, S., Manninen, M., HUTTUNEN, M. O., Kaprio, J. A., Lönnqvist, J. K., O’Neill, J., & Cannon, T. D. (2008) · Molecular Psychiatry · doi:10.1038/mp.2008.87 · Cited by 127 · see citing works
N-acetylcysteine normalizes neurochemical changes in the glutathione-deficient schizophrenia mouse model during development
das Neves Duarte, J. M., Kulak, A., Gholam-Razaee, M. M., Cuenod, M., Gruetter, R., & Do, K. Q. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.07.035 · Cited by 124 · see citing works
Assessments of Function and Biochemistry of the Anterior Cingulate Cortex in Schizophrenia
Reid, M. A., Stoeckel, L. E., White, D. M., Avsar, K. B., Bolding, M., Akella, N. S., Knowlton, R. C., den Hollander, J. A., & Lahti, A. C. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.04.013 · Cited by 122 · see citing works
Age, plasticity, and homeostasis in childhood brain disorders
Dennis, M., Spiegler, B. J., Juranek, J. J., Bigler, E. D., Snead, O. C., & Fletcher, J. M. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.09.010 · Cited by 119 · see citing works
Cognitive impairment and in vivo metabolites in first-episode neuroleptic-naive and chronic medicated schizophrenic patients: a proton magnetic resonance spectroscopy study
Ohrmann, P., Siegmund, A., Suslow, T., Pedersen, A., Spitzberg, K., Kersting, A., Rothermundt, M., Arolt, V., Heindel, W., & Pfleiderer, B. (2007) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2006.07.002 · Cited by 116 · see citing works
Ethyl-Eicosapentaenoic Acid in First-Episode Psychosis. A 1H-MRS Study
Berger, G. E., Wood, S. J., Wellard, R. M., Proffitt, T., McConchie, M., Amminger, G. P., Jackson, G. D., Velakoulis, D., Pantelis, C., & McGorry, P. D. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301628 · Cited by 116 · see citing works
Hippocampal pathology in individuals at ultra-high risk for psychosis: A multi-modal magnetic resonance study
Wood, S. J., Kennedy, D., Phillips, L., Seal, M. L., Yücel, M., Nelson, B., Yung, A. R., Jackson, G. D., McGorry, P. D., Velakoulis, D., et al. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.04.012 · Cited by 114 · see citing works
Online effects of transcranial direct current stimulation in real time on human prefrontal and striatal metabolites
Hone-Blanchet, A., Edden, R. A., & Fecteau, S. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.11.008 · Cited by 110 · see citing works
Updated meta-analyses reveal thalamus volume reduction in patients with first-episode and chronic schizophrenia
Adriano, F., Spoletini, I., Caltagirone, C., & Spalletta, G. (2010) · Schizophrenia Research · doi:10.1016/j.schres.2010.07.007 · Cited by 110 · see citing works
Research Applications of Magnetic Resonance Spectroscopy to Investigate Psychiatric Disorders
Dager, S. R., Corrigan, N. M., Richards, T. L., & Posse, S. (2008) · Topics in Magnetic Resonance Imaging · doi:10.1097/rmr.0b013e318181e0be · Cited by 107 · see citing works
Decreases in ganglion cell layer and inner plexiform layer volumes correlate better with disease severity in schizophrenia patients than retinal nerve fiber layer thickness: Findings from spectral optic coherence tomography
Çelik, M., Kalenderoğlu, A., Karadağ, A. S., Eğilmez, O. B., Almış, B. H., & Şimşek, A. (2016) · European Psychiatry · doi:10.1016/j.eurpsy.2015.10.006 · Cited by 109 · see citing works
Alterations of the occipital lobe in schizophrenia
Tohid, H., Faizan, M., & Faizan, U. (2015) · Neurosciences · doi:10.17712/nsj.2015.3.20140757 · Cited by 108 · see citing works
Neuroimaging and treatment evidence for clinical staging in psychotic disorders: from the at-risk mental state to chronic schizophrenia.
Wood, S., Yung, A., McGorry, P., & Pantelis, C. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.05.034 · Cited by 124 · see citing works
Specific metabolites in the medial prefrontal cortex are associated with the neurocognitive deficits in schizophrenia: A preliminary study
Shirayama, Y., Obata, T., Matsuzawa, D., Nonaka, H., Kanazawa, Y., Yoshitome, E., Ikehira, H., Hashimoto, K., & Iyo, M. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.10.031 · Cited by 103 · see citing works
Update on the Use of MR for Assessment and Diagnosis of Psychiatric Diseases
Agarwal, N., Port, J. D., Bazzocchi, M., & Renshaw, P. F. (2010) · Radiology · doi:10.1148/radiol.09090339 · Cited by 102 · see citing works
Brain Metabolite Abnormalities in the White Matter of Elderly Schizophrenic Subjects: Implication for Glial Dysfunction
Chang, L., Friedman, J. I., Ernst, T., Zhong, K., Tsopelas, N. D., & Davis, K. L. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.05.025 · Cited by 101 · see citing works
Reduced Frontal Glutamate + Glutamine and N-Acetylaspartate Levels in Patients With Chronic Schizophrenia but not in Those at Clinical High Risk for Psychosis or With First-Episode Schizophrenia
Natsubori, T., Inoue, H., Abe, O., Takano, Y., Iwashiro, N., Aoki, Y. Y., Koike, S., Yahata, N., Katsura, M., Gonoi, W., et al. (2013) · Schizophrenia Bulletin · doi:10.1093/schbul/sbt124 · Cited by 100 · see citing works
Resting-State Perfusion in Nonmedicated Schizophrenic Patients: A Continuous Arterial Spin-labeling 3.0-T MR Study
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Proton Magnetic Resonance Spectroscopy of Brains in First-episode Schizophrenic Patients
Guo, Q. (2006)

Authors: Steen, R. G., Hamer, R. M., & Lieberman, J. A.
Affiliations: University of North Carolina at Chapel Hill (US)
Corresponding author: Steen, R Grant
ORCID: Steen, R Grant
Lieberman, Jeffrey A
Venue: Neuropsychopharmacology
Publisher: Springer Science and Business Media LLC
Published: 2005-08-10
Volume: 30
Issue: 11
Pages: 1949-1962
ISSN: 0893-133X (ISSN-L)
1740-634X
DOI: 10.1038/sj.npp.1300850
OpenAlex: W1965782412
Cited by: 254
References: 107
Citations by year: 2025: 4 · 2024: 2 · 2023: 6 · 2022: 4 · 2021: 10 · 2020: 7 · 2019: 6 · 2018: 9 · 2017: 7 · 2016: 10 · 2015: 21 · 2014: 16 · 2013: 27 · 2012: 14
FWCI: 2.02
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Neuropsychopharmacology (publishedVersion)
PubMed (publishedVersion)
Funders: National Alliance for Research on Schizophrenia and Depression
Foundation of Hope for Research and Treatment of Mental Illness
University of North Carolina at Chapel Hill
National Institute of Mental Health (MH-64065, R01MH061603, P50MH064065, MH 61603)
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, brain metabolites, 1H NMR, hippocampus, frontal lobe, cortical gray matter, white matter, chronic schizophrenia, first-episode schizophrenia
MeSH terms: Aspartic Acid, Brain Chemistry, Humans, Magnetic Resonance Spectroscopy, Schizophrenia, Tritium

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Measurement of brain metabolites by 1H magnetic resonance spectroscopy in patients with schizophrenia: a systematic review and meta-analysis

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