Association between cytokine levels, verbal memory and hippocampus volume in psychotic disorders and healthy controls

Objective We investigated whether elevated plasma levels of immune markers were associated with verbal memory and hippocampal subfield volumes in patients with severe mental illnesses and in healthy controls. Method In total, 230 patients with a broad DSM‐IV schizophrenia spectrum illness or bipolar...

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Published inActa psychiatrica Scandinavica Vol. 133; no. 1; pp. 53 - 62
Main Authors Hoseth, E. Z., Westlye, L. T., Hope, S., Dieset, I., Aukrust, P., Melle, I., Haukvik, U. K., Agartz, I., Ueland, T., Andreassen, O. A.
Format Journal Article
LanguageEnglish
Published United States Blackwell Publishing Ltd 01.01.2016
Munksgaard Forlag
Subjects
Online AccessGet full text
ISSN0001-690X
1600-0447
1600-0447
DOI10.1111/acps.12467

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Abstract Objective We investigated whether elevated plasma levels of immune markers were associated with verbal memory and hippocampal subfield volumes in patients with severe mental illnesses and in healthy controls. Method In total, 230 patients with a broad DSM‐IV schizophrenia spectrum illness or bipolar disorder and 236 healthy controls were recruited. Memory was assessed using the Wechsler Memory Scale‐Third Edition (WMS‐III) Logical Memory immediate and delayed recall, and the California Verbal Learning Test summed recall over learning list (CVLT learning) and delayed free recall. We measured plasma levels of soluble tumor necrosis factor receptor 1 (sTNF‐R1), interleukin‐1 receptor antagonist, interleukin‐6, von Willebrand factor, osteoprotegerin, high‐sensitivity C‐reactive protein and sCD40 ligand. Hippocampal subfield estimates were obtained using FreeSurfer. Results We found a moderate negative association between sTNF‐R1 and performance on verbal memory learning and recall tests as measured by the WMS‐III Logical Memory after controlling for age, sex and diagnosis. We observed no interaction effect of diagnosis and sTNF‐R1 on memory scores. We also found a nominally significant positive association between CVLT learning and hippocampal volumes. Conclusion The findings suggest a role for immune involvement in memory independent of severe mental disorders and may support the ‘bigger is better’ hypothesis of hippocampal subfield volumes.
AbstractList Objective: We investigated whether elevated plasma levels of immune markers were associated with verbal memory and hippocampal subfield volumes in patients with severe mental illnesses and in healthy controls. Method: 230 patients with a broad DSM-IV schizophrenia spectrum illness or bipolar disorder and 236 healthy controls were recruited. Memory was assessed using the Wechsler Memory ScaleThird Edition (WMS-III) Logical Memory immediate and delayed recall, and the California Verbal Learning Test summed recall over learning list (CVLT learning) and delayed free recall. We measured plasma levels of soluble tumor necrosis factor receptor 1 (sTNF-R1), interleukin-1 receptor antagonist, interleukin-6, von Willebrand factor, osteoprotegerin, high-sensitivity Creactive protein and sCD40 Ligand. Hippocampal subfield estimates were obtained using FreeSurfer. Results: We found a moderate negative association between sTNF-R1 and performance on verbal memory learning and recall tests as measured by the WMS-III Logical Memory after controlling for age, sex and diagnosis. We observed no interaction effect of diagnosis and sTNF-R1 on memory scores. We also found a nominally significant positive association between CVLT learning and hippocampal volumes. Conclusions: The findings suggest a role for immune involvement in memory independent of severe mental disorders, and may support the “bigger is better” hypothesis of hippocampal subfield volumes.
Objective We investigated whether elevated plasma levels of immune markers were associated with verbal memory and hippocampal subfield volumes in patients with severe mental illnesses and in healthy controls. Method In total, 230 patients with a broad DSM‐IV schizophrenia spectrum illness or bipolar disorder and 236 healthy controls were recruited. Memory was assessed using the Wechsler Memory Scale‐Third Edition (WMS‐III) Logical Memory immediate and delayed recall, and the California Verbal Learning Test summed recall over learning list (CVLT learning) and delayed free recall. We measured plasma levels of soluble tumor necrosis factor receptor 1 (sTNF‐R1), interleukin‐1 receptor antagonist, interleukin‐6, von Willebrand factor, osteoprotegerin, high‐sensitivity C‐reactive protein and sCD40 ligand. Hippocampal subfield estimates were obtained using FreeSurfer. Results We found a moderate negative association between sTNF‐R1 and performance on verbal memory learning and recall tests as measured by the WMS‐III Logical Memory after controlling for age, sex and diagnosis. We observed no interaction effect of diagnosis and sTNF‐R1 on memory scores. We also found a nominally significant positive association between CVLT learning and hippocampal volumes. Conclusion The findings suggest a role for immune involvement in memory independent of severe mental disorders and may support the ‘bigger is better’ hypothesis of hippocampal subfield volumes.
Objective We investigated whether elevated plasma levels of immune markers were associated with verbal memory and hippocampal subfield volumes in patients with severe mental illnesses and in healthy controls. Method In total, 230 patients with a broad DSM-IV schizophrenia spectrum illness or bipolar disorder and 236 healthy controls were recruited. Memory was assessed using the Wechsler Memory Scale-Third Edition (WMS-III) Logical Memory immediate and delayed recall, and the California Verbal Learning Test summed recall over learning list (CVLT learning) and delayed free recall. We measured plasma levels of soluble tumor necrosis factor receptor 1 (sTNF-R1), interleukin-1 receptor antagonist, interleukin-6, von Willebrand factor, osteoprotegerin, high-sensitivity C-reactive protein and sCD40 ligand. Hippocampal subfield estimates were obtained using FreeSurfer. Results We found a moderate negative association between sTNF-R1 and performance on verbal memory learning and recall tests as measured by the WMS-III Logical Memory after controlling for age, sex and diagnosis. We observed no interaction effect of diagnosis and sTNF-R1 on memory scores. We also found a nominally significant positive association between CVLT learning and hippocampal volumes. Conclusion The findings suggest a role for immune involvement in memory independent of severe mental disorders and may support the 'bigger is better' hypothesis of hippocampal subfield volumes.
We investigated whether elevated plasma levels of immune markers were associated with verbal memory and hippocampal subfield volumes in patients with severe mental illnesses and in healthy controls.OBJECTIVEWe investigated whether elevated plasma levels of immune markers were associated with verbal memory and hippocampal subfield volumes in patients with severe mental illnesses and in healthy controls.In total, 230 patients with a broad DSM-IV schizophrenia spectrum illness or bipolar disorder and 236 healthy controls were recruited. Memory was assessed using the Wechsler Memory Scale-Third Edition (WMS-III) Logical Memory immediate and delayed recall, and the California Verbal Learning Test summed recall over learning list (CVLT learning) and delayed free recall. We measured plasma levels of soluble tumor necrosis factor receptor 1 (sTNF-R1), interleukin-1 receptor antagonist, interleukin-6, von Willebrand factor, osteoprotegerin, high-sensitivity C-reactive protein and sCD40 ligand. Hippocampal subfield estimates were obtained using FreeSurfer.METHODIn total, 230 patients with a broad DSM-IV schizophrenia spectrum illness or bipolar disorder and 236 healthy controls were recruited. Memory was assessed using the Wechsler Memory Scale-Third Edition (WMS-III) Logical Memory immediate and delayed recall, and the California Verbal Learning Test summed recall over learning list (CVLT learning) and delayed free recall. We measured plasma levels of soluble tumor necrosis factor receptor 1 (sTNF-R1), interleukin-1 receptor antagonist, interleukin-6, von Willebrand factor, osteoprotegerin, high-sensitivity C-reactive protein and sCD40 ligand. Hippocampal subfield estimates were obtained using FreeSurfer.We found a moderate negative association between sTNF-R1 and performance on verbal memory learning and recall tests as measured by the WMS-III Logical Memory after controlling for age, sex and diagnosis. We observed no interaction effect of diagnosis and sTNF-R1 on memory scores. We also found a nominally significant positive association between CVLT learning and hippocampal volumes.RESULTSWe found a moderate negative association between sTNF-R1 and performance on verbal memory learning and recall tests as measured by the WMS-III Logical Memory after controlling for age, sex and diagnosis. We observed no interaction effect of diagnosis and sTNF-R1 on memory scores. We also found a nominally significant positive association between CVLT learning and hippocampal volumes.The findings suggest a role for immune involvement in memory independent of severe mental disorders and may support the 'bigger is better' hypothesis of hippocampal subfield volumes.CONCLUSIONThe findings suggest a role for immune involvement in memory independent of severe mental disorders and may support the 'bigger is better' hypothesis of hippocampal subfield volumes.
We investigated whether elevated plasma levels of immune markers were associated with verbal memory and hippocampal subfield volumes in patients with severe mental illnesses and in healthy controls. In total, 230 patients with a broad DSM-IV schizophrenia spectrum illness or bipolar disorder and 236 healthy controls were recruited. Memory was assessed using the Wechsler Memory Scale-Third Edition (WMS-III) Logical Memory immediate and delayed recall, and the California Verbal Learning Test summed recall over learning list (CVLT learning) and delayed free recall. We measured plasma levels of soluble tumor necrosis factor receptor 1 (sTNF-R1), interleukin-1 receptor antagonist, interleukin-6, von Willebrand factor, osteoprotegerin, high-sensitivity C-reactive protein and sCD40 ligand. Hippocampal subfield estimates were obtained using FreeSurfer. We found a moderate negative association between sTNF-R1 and performance on verbal memory learning and recall tests as measured by the WMS-III Logical Memory after controlling for age, sex and diagnosis. We observed no interaction effect of diagnosis and sTNF-R1 on memory scores. We also found a nominally significant positive association between CVLT learning and hippocampal volumes. The findings suggest a role for immune involvement in memory independent of severe mental disorders and may support the 'bigger is better' hypothesis of hippocampal subfield volumes.
Author Westlye, L. T.
Hope, S.
Ueland, T.
Agartz, I.
Hoseth, E. Z.
Melle, I.
Haukvik, U. K.
Andreassen, O. A.
Dieset, I.
Aukrust, P.
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/26189721$$D View this record in MEDLINE/PubMed
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Issue 1
Keywords psychoses
neurocognition
neuroimaging
Language English
License http://onlinelibrary.wiley.com/termsAndConditions#vor
2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.
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Table S1. Demographic and clinical characteristics of participants in the MRI subgroup (N = 224). Table S2. Immune and verbal memory characteristics for the Main group (N = 462). Table S3. Immune, verbal memory and hippocampal volume characteristics for the MRI subgroup (N = 224). Table S4. Linear regression models investigating the associations between verbal memory and cytokines in whole sample (N = 462) after controlling for age, sex and diagnosis. Table S5. Linear regression analyses of associations between verbal memory and hippocampal volumes in subsample (N = 224) after controlling for age, sex, estimated total intracranial volume and diagnosis (patient or control). Table S6. Linear regression analyses investigating associations between hippocampal subvolumes and cytokines in MRI subgroup (N = 224) after controlling for age, sex, estimated total intracranial volume and diagnosis (patient or control). Table S7. Spearman's rank correlation between cytokines and time of blood sampling for the control group (N = 174)
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crossref_primary_10_1111_acps_12467
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PublicationCentury 2000
PublicationDate January 2016
PublicationDateYYYYMMDD 2016-01-01
PublicationDate_xml – month: 01
  year: 2016
  text: January 2016
PublicationDecade 2010
PublicationPlace United States
PublicationPlace_xml – name: United States
– name: Aalborg
PublicationTitle Acta psychiatrica Scandinavica
PublicationTitleAlternate Acta Psychiatr Scand
PublicationYear 2016
Publisher Blackwell Publishing Ltd
Munksgaard Forlag
Publisher_xml – name: Blackwell Publishing Ltd
– name: Munksgaard Forlag
References Fischl B. FreeSurfer. NeuroImage 2012;62:774-781.
Rund BR, Sundet K, Asbjornsen A et al. Neuropsychological test profiles in schizophrenia and non-psychotic depression. Acta Psychiatr Scand 2006;113:350-359.
Yirmiya R, Goshen I. Immune modulation of learning, memory, neural plasticity and neurogenesis. Brain Behav Immun 2011;25:181-213.
Steen NE, Lorentzen S, Barrett EA et al. Sex-specific cortisol levels in bipolar disorder and schizophrenia during mental challenge-relationship to clinical characteristics and medication. Prog Neuropsychopharmacol Biol Psychiatry 2011;35:1100-1107.
Shi J, Levinson DF, Duan J et al. Common variants on chromosome 6p22.1 are associated with schizophrenia. Nature 2009;460:753-757.
Mueller SG, Weiner MW. Selective effect of age, Apo e4, and Alzheimer's disease on hippocampal subfields. Hippocampus 2009;19:558-564.
Munkholm K, Brauner JV, Kessing LV, Vinberg M. Cytokines in bipolar disorder vs. healthy control subjects: a systematic review and meta-analysis. J Psychiatr Res 2013;47:1119-1133.
Tamminga CA, Stan AD, Wagner AD. The hippocampal formation in schizophrenia. Am J Psychiatry 2010;167:1178-1193.
Tischler L, Brand SR, Stavitsky K et al. The relationship between hippocampal volume and declarative memory in a population of combat veterans with and without PTSD. Ann N Y Acad Sci 2006;1071:405-409.
Craddock N, Sklar P. Genetics of bipolar disorder. Lancet 2013;381:1654-1662.
Tesli M, Espeseth T, Bettella F et al. Polygenic risk score and the psychosis continuum model. Acta Psychiatr Scand 2014;130:311-317.
Fischl B, Salat DH, Busa E et al. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 2002;33:341-355.
Drew PD, Lonergan M, Goldstein ME, Lampson LA, Ozato K, McFarlin DE. Regulation of MHC class I and beta 2-microglobulin gene expression in human neuronal cells. Factor binding to conserved cis-acting regulatory sequences correlates with expression of the genes. J Immunol 1993;1:3300-3310.
Wechsler D, Wycherley RJ, Benjamin L. Wechsler Memory Scale: WMS-III. Stockholm, Sweden: Pearson Assessment; 2008.
Seguin JA, Brennan J, Mangano E, Hayley S. Proinflammatory cytokines differentially influence adult hippocampal cell proliferation depending upon the route and chronicity of administration. Neuropsychiatr Dis Treat 2009;5:5-14.
Reuter M, Rosas HD, Fischl B. Highly accurate inverse consistent registration: a robust approach. NeuroImage 2010;53:1181-1196.
Haukvik UK, Westlye LT, Mørch-Johnsen L et al. In vivo hippocampal subfield volumes in schizophrenia and bipolar disorder. Biol Psychiatry 2015;77:581-588.
Simonsen C, Sundet K, Vaskinn A et al. Neurocognitive dysfunction in bipolar and schizophrenia spectrum disorders depends on history of psychosis rather than diagnostic group. Schizophr Bull 2011;37:73-83.
McAfoose J, Baune BT. Evidence for a cytokine model of cognitive function. Neurosci Biobehav Rev 2009;33:355-366.
Wu MD, Hein AM, Moravan MJ, Shaftel SS, Olschowka JA, O'Banion MK. Adult murine hippocampal neurogenesis is inhibited by sustained IL-1beta and not rescued by voluntary running. Brain Behav Immun 2012;26:292-300.
Shimamura M, Nakagami H, Osako MK et al. OPG/RANKL/RANK axis is a critical inflammatory signaling system in ischemic brain in mice. Proc Natl Acad Sci USA 2014;111:8191-8196.
Segonne F, Dale AM, Busa E et al. A hybrid approach to the skull stripping problem in MRI. NeuroImage 2004;22:1060-1075.
Cardno AG, Owen MJ. Genetic relationships between schizophrenia, bipolar disorder, and schizoaffective disorder. Schizophr Bull 2014;40:504-515.
Chepenik LG, Wang F, Spencer L et al. Structure-function associations in hippocampus in bipolar disorder. Biol Psychol 2012;90:18-22.
Kesler S, Janelsins M, Koovakkattu D et al. Reduced hippocampal volume and verbal memory performance associated with interleukin-6 and tumor necrosis factor-alpha levels in chemotherapy-treated breast cancer survivors. Brain Behav Immun 2013;30(Suppl):S109-S116.
Fischl B, Salat DH, van der Kouwe AJ et al. Sequence-independent segmentation of magnetic resonance images. NeuroImage 2004;23(Suppl 1):S69-S84.
Jones KA, Thomsen C. The role of the innate immune system in psychiatric disorders. Mol Cell Neurosci 2013;53:52-62.
de Miranda AS, Brant F, Campos AC et al. Evidence for the contribution of adult neurogenesis and hippocampal cell death in experimental cerebral malaria cognitive outcome. Neuroscience 2015;284:920-933.
Hope S, Ueland T, Steen NE et al. Interleukin 1 receptor antagonist and soluble tumor necrosis factor receptor 1 are associated with general severity and psychotic symptoms in schizophrenia and bipolar disorder. Schizophr Res 2013;145:36-42.
Hamdani N, Doukhan R, Kurtlucan O, Tamouza R, Leboyer M. Immunity, inflammation, and bipolar disorder: diagnostic and therapeutic implications. Curr Psychiatry Rep 2013;15:387.
Hufner K, Kandler C, Koudouovoh-Tripp P et al. Bioprofiling of platelets in medicated patients with depression. J Affect Disord 2014;172c:81-88.
Arisi GM. Nervous and immune systems signals and connections: Cytokines in hippocampus physiology and pathology. Epilepsy Behav 2014;38:43-47.
Van Leemput K, Bakkour A, Benner T et al. Automated segmentation of hippocampal subfields from ultra-high resolution in vivo MRI. Hippocampus 2009;19:549-557.
Schizophrenia Psychiatric Genome-Wide Association Study (GWAS) Consortium. Genome-wide association study identifies five new schizophrenia loci. Nat Genet 2011;43:969-976.
Hope S, Melle I, Aukrust P et al. Osteoprotegerin levels in patients with severe mental disorders. J Psychiatry Neurosci 2010;35:304-310.
Verma S, Nakaoke R, Dohgu S, Banks WA. Release of cytokines by brain endothelial cells: a polarized response to lipopolysaccharide. Brain Behav Immun 2006;20:449-455.
Rimol LM, Hartberg CB, Nesvag R et al. Cortical thickness and subcortical volumes in schizophrenia and bipolar disorder. Biol Psychiatry 2010;68:41-50.
Nelson PA, Sage JR, Wood SC, Davenport CM, Anagnostaras SG, Boulanger LM. MHC class I immune proteins are critical for hippocampus-dependent memory and gate NMDAR-dependent hippocampal long-term depression. Learn Mem 2013;20:505-517.
Elmer BM, McAllister AK. Major histocompatibility complex class I proteins in brain development and plasticity. Trends Neurosci 2012;35:660-670.
Schulz KF, Grimes DA. Multiplicity in randomised trials I: endpoints and treatments. Lancet 2005;365:1591-1595.
Delis DC, Kramer JH, Kaplan E, Ober BA. California Verbal Learning Test: CVLT-II. Stockholm, Sweden: Pearson Assessment; 2004.
Ringen PA, Engh JA, Birkenaes AB, Dieset I, Andreassen OA. Increased mortality in schizophrenia due to cardiovascular disease - a non-systematic review of epidemiology, possible causes, and interventions. Front Psychiatry 2014;5:137.
Grande I, Magalhaes PV, Chendo I et al. Staging bipolar disorder: clinical, biochemical, and functional correlates. Acta Psychiatr Scand 2014;129:437-444.
Altamura AC, Pozzoli S, Fiorentini A, Dell'osso B. Neurodevelopment and inflammatory patterns in schizophrenia in relation to pathophysiology. Prog Neuropsychopharmacol Biol Psychiatry 2013;42:63-70.
Hudetz JA, Gandhi SD, Iqbal Z, Patterson KM, Pagel PS. Elevated postoperative inflammatory biomarkers are associated with short- and medium-term cognitive dysfunction after coronary artery surgery. J Anesth 2011;25:1-9.
Mathew I, Gardin TM, Tandon N et al. Medial Temporal Lobe Structures and Hippocampal Subfields in Psychotic Disorders: findings From the Bipolar-Schizophrenia Network on Intermediate Phenotypes (B-SNIP) Study. JAMA Psychiatry 2014;71:769-777.
Butler MP, O'Connor JJ, Moynagh PN. Dissection of tumor-necrosis factor-alpha inhibition of long-term potentiation (LTP) reveals a p38 mitogen-activated protein kinase-dependent mechanism which maps to early-but not late-phase LTP. Neuroscience 2004;124:319-326.
Mavroudis PD, Scheff JD, Calvano SE, Androulakis IP. Systems biology of circadian-immune interactions. J Innate Immun 2013;5:153-162.
Hope S, Dieset I, Agartz I et al. Affective symptoms are associated with markers of inflammation and immune activation in bipolar disorders but not in schizophrenia. J Psychiatr Res 2011;45:1608-1616.
Hope S, Melle I, Aukrust P et al. Similar immune profile in bipolar disorder and schizophrenia: selective increase in soluble tumor necrosis factor receptor I and von Willebrand factor. Bipolar Disord 2009;11:726-734.
Erickson MA, Dohi K, Banks WA. Neuroinflammation: a common pathway in CNS diseases as mediated at the blood-brain barrier. NeuroImmunoModulation 2012;19:121-130.
Shatz CJ. MHC class I: an unexpected role in neuronal plasticity. Neuron 2009;64:40-45.
Steen NE, Methlie P, Lorentzen S et al. Altered systemic cortisol metabolism in bipolar disorder and schizophrenia spectrum disorders. J Psychiatr Res 2014;52:57-62.
Bourne C, Aydemir O, Balanza-Martinez V et al. Neuropsychological testing of cognitive impairment in euthymic bipolar disorder: an individual patient data meta-analysis. Acta Psychiatr Scand 2013;128:149-162.
Steen NE, Methlie P, Lorentzen S et al. Increased systemic cortisol metabolism in patients with schizophrenia and bipolar disorder: a mechanism for increased stress vulnerability? J Clin Psychiatry 2011;72:1515-1521.
van Dongen J, Boomsma DI. The evolutionary paradox and the missing heritability of schizophrenia. Am J Med Genet B Neuropsychiatr Genet 2013;162b:122-136.
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2010; 53
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2010; 35
2009; 64
2013; 42
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2002; 33
2013; 145
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2013; 162b
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Hufner K (e_1_2_9_23_1) 2014; 172
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References_xml – reference: Jones KA, Thomsen C. The role of the innate immune system in psychiatric disorders. Mol Cell Neurosci 2013;53:52-62.
– reference: Wu MD, Hein AM, Moravan MJ, Shaftel SS, Olschowka JA, O'Banion MK. Adult murine hippocampal neurogenesis is inhibited by sustained IL-1beta and not rescued by voluntary running. Brain Behav Immun 2012;26:292-300.
– reference: Hope S, Dieset I, Agartz I et al. Affective symptoms are associated with markers of inflammation and immune activation in bipolar disorders but not in schizophrenia. J Psychiatr Res 2011;45:1608-1616.
– reference: Grande I, Magalhaes PV, Chendo I et al. Staging bipolar disorder: clinical, biochemical, and functional correlates. Acta Psychiatr Scand 2014;129:437-444.
– reference: Steen NE, Lorentzen S, Barrett EA et al. Sex-specific cortisol levels in bipolar disorder and schizophrenia during mental challenge-relationship to clinical characteristics and medication. Prog Neuropsychopharmacol Biol Psychiatry 2011;35:1100-1107.
– reference: Mathew I, Gardin TM, Tandon N et al. Medial Temporal Lobe Structures and Hippocampal Subfields in Psychotic Disorders: findings From the Bipolar-Schizophrenia Network on Intermediate Phenotypes (B-SNIP) Study. JAMA Psychiatry 2014;71:769-777.
– reference: Shatz CJ. MHC class I: an unexpected role in neuronal plasticity. Neuron 2009;64:40-45.
– reference: Hope S, Ueland T, Steen NE et al. Interleukin 1 receptor antagonist and soluble tumor necrosis factor receptor 1 are associated with general severity and psychotic symptoms in schizophrenia and bipolar disorder. Schizophr Res 2013;145:36-42.
– reference: Fischl B, Salat DH, Busa E et al. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 2002;33:341-355.
– reference: Fischl B, Salat DH, van der Kouwe AJ et al. Sequence-independent segmentation of magnetic resonance images. NeuroImage 2004;23(Suppl 1):S69-S84.
– reference: Butler MP, O'Connor JJ, Moynagh PN. Dissection of tumor-necrosis factor-alpha inhibition of long-term potentiation (LTP) reveals a p38 mitogen-activated protein kinase-dependent mechanism which maps to early-but not late-phase LTP. Neuroscience 2004;124:319-326.
– reference: Verma S, Nakaoke R, Dohgu S, Banks WA. Release of cytokines by brain endothelial cells: a polarized response to lipopolysaccharide. Brain Behav Immun 2006;20:449-455.
– reference: Fischl B. FreeSurfer. NeuroImage 2012;62:774-781.
– reference: Munkholm K, Brauner JV, Kessing LV, Vinberg M. Cytokines in bipolar disorder vs. healthy control subjects: a systematic review and meta-analysis. J Psychiatr Res 2013;47:1119-1133.
– reference: Cardno AG, Owen MJ. Genetic relationships between schizophrenia, bipolar disorder, and schizoaffective disorder. Schizophr Bull 2014;40:504-515.
– reference: Tamminga CA, Stan AD, Wagner AD. The hippocampal formation in schizophrenia. Am J Psychiatry 2010;167:1178-1193.
– reference: Craddock N, Sklar P. Genetics of bipolar disorder. Lancet 2013;381:1654-1662.
– reference: van Dongen J, Boomsma DI. The evolutionary paradox and the missing heritability of schizophrenia. Am J Med Genet B Neuropsychiatr Genet 2013;162b:122-136.
– reference: Steen NE, Methlie P, Lorentzen S et al. Altered systemic cortisol metabolism in bipolar disorder and schizophrenia spectrum disorders. J Psychiatr Res 2014;52:57-62.
– reference: Van Leemput K, Bakkour A, Benner T et al. Automated segmentation of hippocampal subfields from ultra-high resolution in vivo MRI. Hippocampus 2009;19:549-557.
– reference: Delis DC, Kramer JH, Kaplan E, Ober BA. California Verbal Learning Test: CVLT-II. Stockholm, Sweden: Pearson Assessment; 2004.
– reference: Reuter M, Rosas HD, Fischl B. Highly accurate inverse consistent registration: a robust approach. NeuroImage 2010;53:1181-1196.
– reference: Shi J, Levinson DF, Duan J et al. Common variants on chromosome 6p22.1 are associated with schizophrenia. Nature 2009;460:753-757.
– reference: Seguin JA, Brennan J, Mangano E, Hayley S. Proinflammatory cytokines differentially influence adult hippocampal cell proliferation depending upon the route and chronicity of administration. Neuropsychiatr Dis Treat 2009;5:5-14.
– reference: Schizophrenia Psychiatric Genome-Wide Association Study (GWAS) Consortium. Genome-wide association study identifies five new schizophrenia loci. Nat Genet 2011;43:969-976.
– reference: Hope S, Melle I, Aukrust P et al. Osteoprotegerin levels in patients with severe mental disorders. J Psychiatry Neurosci 2010;35:304-310.
– reference: Ringen PA, Engh JA, Birkenaes AB, Dieset I, Andreassen OA. Increased mortality in schizophrenia due to cardiovascular disease - a non-systematic review of epidemiology, possible causes, and interventions. Front Psychiatry 2014;5:137.
– reference: Shimamura M, Nakagami H, Osako MK et al. OPG/RANKL/RANK axis is a critical inflammatory signaling system in ischemic brain in mice. Proc Natl Acad Sci USA 2014;111:8191-8196.
– reference: Kesler S, Janelsins M, Koovakkattu D et al. Reduced hippocampal volume and verbal memory performance associated with interleukin-6 and tumor necrosis factor-alpha levels in chemotherapy-treated breast cancer survivors. Brain Behav Immun 2013;30(Suppl):S109-S116.
– reference: Schulz KF, Grimes DA. Multiplicity in randomised trials I: endpoints and treatments. Lancet 2005;365:1591-1595.
– reference: Mavroudis PD, Scheff JD, Calvano SE, Androulakis IP. Systems biology of circadian-immune interactions. J Innate Immun 2013;5:153-162.
– reference: Altamura AC, Pozzoli S, Fiorentini A, Dell'osso B. Neurodevelopment and inflammatory patterns in schizophrenia in relation to pathophysiology. Prog Neuropsychopharmacol Biol Psychiatry 2013;42:63-70.
– reference: Steen NE, Methlie P, Lorentzen S et al. Increased systemic cortisol metabolism in patients with schizophrenia and bipolar disorder: a mechanism for increased stress vulnerability? J Clin Psychiatry 2011;72:1515-1521.
– reference: Erickson MA, Dohi K, Banks WA. Neuroinflammation: a common pathway in CNS diseases as mediated at the blood-brain barrier. NeuroImmunoModulation 2012;19:121-130.
– reference: Rund BR, Sundet K, Asbjornsen A et al. Neuropsychological test profiles in schizophrenia and non-psychotic depression. Acta Psychiatr Scand 2006;113:350-359.
– reference: Bourne C, Aydemir O, Balanza-Martinez V et al. Neuropsychological testing of cognitive impairment in euthymic bipolar disorder: an individual patient data meta-analysis. Acta Psychiatr Scand 2013;128:149-162.
– reference: Segonne F, Dale AM, Busa E et al. A hybrid approach to the skull stripping problem in MRI. NeuroImage 2004;22:1060-1075.
– reference: Hudetz JA, Gandhi SD, Iqbal Z, Patterson KM, Pagel PS. Elevated postoperative inflammatory biomarkers are associated with short- and medium-term cognitive dysfunction after coronary artery surgery. J Anesth 2011;25:1-9.
– reference: McAfoose J, Baune BT. Evidence for a cytokine model of cognitive function. Neurosci Biobehav Rev 2009;33:355-366.
– reference: Tesli M, Espeseth T, Bettella F et al. Polygenic risk score and the psychosis continuum model. Acta Psychiatr Scand 2014;130:311-317.
– reference: Nelson PA, Sage JR, Wood SC, Davenport CM, Anagnostaras SG, Boulanger LM. MHC class I immune proteins are critical for hippocampus-dependent memory and gate NMDAR-dependent hippocampal long-term depression. Learn Mem 2013;20:505-517.
– reference: Tischler L, Brand SR, Stavitsky K et al. The relationship between hippocampal volume and declarative memory in a population of combat veterans with and without PTSD. Ann N Y Acad Sci 2006;1071:405-409.
– reference: Wechsler D, Wycherley RJ, Benjamin L. Wechsler Memory Scale: WMS-III. Stockholm, Sweden: Pearson Assessment; 2008.
– reference: Mueller SG, Weiner MW. Selective effect of age, Apo e4, and Alzheimer's disease on hippocampal subfields. Hippocampus 2009;19:558-564.
– reference: Hufner K, Kandler C, Koudouovoh-Tripp P et al. Bioprofiling of platelets in medicated patients with depression. J Affect Disord 2014;172c:81-88.
– reference: Rimol LM, Hartberg CB, Nesvag R et al. Cortical thickness and subcortical volumes in schizophrenia and bipolar disorder. Biol Psychiatry 2010;68:41-50.
– reference: Arisi GM. Nervous and immune systems signals and connections: Cytokines in hippocampus physiology and pathology. Epilepsy Behav 2014;38:43-47.
– reference: Simonsen C, Sundet K, Vaskinn A et al. Neurocognitive dysfunction in bipolar and schizophrenia spectrum disorders depends on history of psychosis rather than diagnostic group. Schizophr Bull 2011;37:73-83.
– reference: Yirmiya R, Goshen I. Immune modulation of learning, memory, neural plasticity and neurogenesis. Brain Behav Immun 2011;25:181-213.
– reference: Hope S, Melle I, Aukrust P et al. Similar immune profile in bipolar disorder and schizophrenia: selective increase in soluble tumor necrosis factor receptor I and von Willebrand factor. Bipolar Disord 2009;11:726-734.
– reference: Drew PD, Lonergan M, Goldstein ME, Lampson LA, Ozato K, McFarlin DE. Regulation of MHC class I and beta 2-microglobulin gene expression in human neuronal cells. Factor binding to conserved cis-acting regulatory sequences correlates with expression of the genes. J Immunol 1993;1:3300-3310.
– reference: Elmer BM, McAllister AK. Major histocompatibility complex class I proteins in brain development and plasticity. Trends Neurosci 2012;35:660-670.
– reference: de Miranda AS, Brant F, Campos AC et al. Evidence for the contribution of adult neurogenesis and hippocampal cell death in experimental cerebral malaria cognitive outcome. Neuroscience 2015;284:920-933.
– reference: Chepenik LG, Wang F, Spencer L et al. Structure-function associations in hippocampus in bipolar disorder. Biol Psychol 2012;90:18-22.
– reference: Haukvik UK, Westlye LT, Mørch-Johnsen L et al. In vivo hippocampal subfield volumes in schizophrenia and bipolar disorder. Biol Psychiatry 2015;77:581-588.
– reference: Hamdani N, Doukhan R, Kurtlucan O, Tamouza R, Leboyer M. Immunity, inflammation, and bipolar disorder: diagnostic and therapeutic implications. Curr Psychiatry Rep 2013;15:387.
– volume: 77
  start-page: 581
  year: 2015
  end-page: 588
  article-title: hippocampal subfield volumes in schizophrenia and bipolar disorder
  publication-title: Biol Psychiatry
– volume: 162b
  start-page: 122
  year: 2013
  end-page: 136
  article-title: The evolutionary paradox and the missing heritability of schizophrenia
  publication-title: Am J Med Genet B Neuropsychiatr Genet
– volume: 11
  start-page: 726
  year: 2009
  end-page: 734
  article-title: Similar immune profile in bipolar disorder and schizophrenia: selective increase in soluble tumor necrosis factor receptor I and von Willebrand factor
  publication-title: Bipolar Disord
– volume: 26
  start-page: 292
  year: 2012
  end-page: 300
  article-title: Adult murine hippocampal neurogenesis is inhibited by sustained IL‐1beta and not rescued by voluntary running
  publication-title: Brain Behav Immun
– volume: 23
  start-page: S69
  issue: Suppl 1
  year: 2004
  end-page: S84
  article-title: Sequence‐independent segmentation of magnetic resonance images
  publication-title: NeuroImage
– volume: 172c
  start-page: 81
  year: 2014
  end-page: 88
  article-title: Bioprofiling of platelets in medicated patients with depression
  publication-title: J Affect Disord
– volume: 68
  start-page: 41
  year: 2010
  end-page: 50
  article-title: Cortical thickness and subcortical volumes in schizophrenia and bipolar disorder
  publication-title: Biol Psychiatry
– volume: 124
  start-page: 319
  year: 2004
  end-page: 326
  article-title: Dissection of tumor‐necrosis factor‐alpha inhibition of long‐term potentiation (LTP) reveals a p38 mitogen‐activated protein kinase‐dependent mechanism which maps to early‐but not late‐phase LTP
  publication-title: Neuroscience
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  year: 2009
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  article-title: Common variants on chromosome 6p22.1 are associated with schizophrenia
  publication-title: Nature
– volume: 53
  start-page: 52
  year: 2013
  end-page: 62
  article-title: The role of the innate immune system in psychiatric disorders
  publication-title: Mol Cell Neurosci
– volume: 33
  start-page: 341
  year: 2002
  end-page: 355
  article-title: Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain
  publication-title: Neuron
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  year: 2011
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  article-title: Increased systemic cortisol metabolism in patients with schizophrenia and bipolar disorder: a mechanism for increased stress vulnerability?
  publication-title: J Clin Psychiatry
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  year: 2013
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  start-page: 437
  year: 2014
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  article-title: Staging bipolar disorder: clinical, biochemical, and functional correlates
  publication-title: Acta Psychiatr Scand
– volume: 90
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  year: 2012
  end-page: 22
  article-title: Structure‐function associations in hippocampus in bipolar disorder
  publication-title: Biol Psychol
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  year: 2011
  end-page: 213
  article-title: Immune modulation of learning, memory, neural plasticity and neurogenesis
  publication-title: Brain Behav Immun
– volume: 25
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  year: 2011
  end-page: 9
  article-title: Elevated postoperative inflammatory biomarkers are associated with short‐ and medium‐term cognitive dysfunction after coronary artery surgery
  publication-title: J Anesth
– volume: 64
  start-page: 40
  year: 2009
  end-page: 45
  article-title: MHC class I: an unexpected role in neuronal plasticity
  publication-title: Neuron
– year: 2008
– volume: 5
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  year: 2013
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Snippet Objective We investigated whether elevated plasma levels of immune markers were associated with verbal memory and hippocampal subfield volumes in patients with...
We investigated whether elevated plasma levels of immune markers were associated with verbal memory and hippocampal subfield volumes in patients with severe...
Objective We investigated whether elevated plasma levels of immune markers were associated with verbal memory and hippocampal subfield volumes in patients with...
Objective: We investigated whether elevated plasma levels of immune markers were associated with verbal memory and hippocampal subfield volumes in patients...
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StartPage 53
SubjectTerms Adolescent
Adult
Bipolar Disorder - blood
Bipolar Disorder - pathology
Bipolar Disorder - psychology
Cytokines
Cytokines - blood
Diffusion Magnetic Resonance Imaging - methods
Female
Hippocampus - pathology
Humans
Male
Memory
Memory - physiology
Mental disorders
Mental Recall - physiology
Middle Aged
neurocognition
neuroimaging
Neuropsychological Tests - standards
Psychopathology
psychoses
Psychotic Disorders - blood
Psychotic Disorders - pathology
Psychotic Disorders - psychology
Schizophrenia - blood
Schizophrenia - pathology
Verbal Learning - physiology
Title Association between cytokine levels, verbal memory and hippocampus volume in psychotic disorders and healthy controls
URI https://api.istex.fr/ark:/67375/WNG-8Z96SWMR-2/fulltext.pdf
https://onlinelibrary.wiley.com/doi/abs/10.1111%2Facps.12467
https://www.ncbi.nlm.nih.gov/pubmed/26189721
https://www.proquest.com/docview/1757078222
https://www.proquest.com/docview/1760875031
https://www.proquest.com/docview/1776667474
http://hdl.handle.net/10852/66220
Volume 133
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