Longitudinal assessment of ventricular volume trajectories in early-stage schizophrenia: evidence of both enlargement and shrinkage
Language English Country Great Britain, England Media electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
PubMed
38658884
PubMed Central
PMC11040899
DOI
10.1186/s12888-024-05749-5
PII: 10.1186/s12888-024-05749-5
Knihovny.cz E-resources
- Keywords
- First-episode schizophrenia, Longitudinal design, MRI, Negative symptoms, Ventricular volumes,
- MeSH
- Adult MeSH
- Humans MeSH
- Longitudinal Studies MeSH
- Magnetic Resonance Imaging * MeSH
- Adolescent MeSH
- Young Adult MeSH
- Cerebral Ventricles diagnostic imaging pathology MeSH
- Disease Progression MeSH
- Schizophrenia * diagnostic imaging pathology physiopathology MeSH
- Case-Control Studies MeSH
- Lateral Ventricles diagnostic imaging pathology MeSH
- Check Tag
- Adult MeSH
- Humans MeSH
- Adolescent MeSH
- Young Adult MeSH
- Male MeSH
- Female MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
BACKGROUND: Lateral ventricular enlargement represents a canonical morphometric finding in chronic patients with schizophrenia; however, longitudinal studies elucidating complex dynamic trajectories of ventricular volume change during critical early disease stages are sparse. METHODS: We measured lateral ventricular volumes in 113 first-episode schizophrenia patients (FES) at baseline visit (11.7 months after illness onset, SD = 12.3) and 128 age- and sex-matched healthy controls (HC) using 3T MRI. MRI was then repeated in both FES and HC one year later. RESULTS: Compared to controls, ventricular enlargement was identified in 18.6% of patients with FES (14.1% annual ventricular volume (VV) increase; 95%CI: 5.4; 33.1). The ventricular expansion correlated with the severity of PANSS-negative symptoms at one-year follow-up (p = 0.0078). Nevertheless, 16.8% of FES showed an opposite pattern of statistically significant ventricular shrinkage during ≈ one-year follow-up (-9.5% annual VV decrease; 95%CI: -23.7; -2.4). There were no differences in sex, illness duration, age of onset, duration of untreated psychosis, body mass index, the incidence of Schneiderian symptoms, or cumulative antipsychotic dose among the patient groups exhibiting ventricular enlargement, shrinkage, or no change in VV. CONCLUSION: Both enlargement and ventricular shrinkage are equally present in the early stages of schizophrenia. The newly discovered early reduction of VV in a subgroup of patients emphasizes the need for further research to understand its mechanisms.
3rd Faculty of Medicine Charles University Prague Czech Republic
National Institute of Mental Health Topolova 748 250 67 Klecany Czech Republic
See more in PubMed
Dietsche B, Kircher T, Falkenberg I. Structural brain changes in schizophrenia at different stages of the illness: a selective review of longitudinal magnetic resonance imaging studies. Aust N Z J Psychiatry. 2017;51(5):500–8. doi: 10.1177/0004867417699473. PubMed DOI
Birur B, Kraguljac NV, Shelton RC, Lahti AC. Brain structure, function, and neurochemistry in schizophrenia and bipolar disorder-a systematic review of the magnetic resonance neuroimaging literature. NPJ Schizophr. 2017;3:15. doi: 10.1038/s41537-017-0013-9. PubMed DOI PMC
Kempton MJ, Stahl D, Williams SC, DeLisi LE. Progressive lateral ventricular enlargement in schizophrenia: a meta-analysis of longitudinal MRI studies. Schizophr Res. 2010;120(1–3):54–62. doi: 10.1016/j.schres.2010.03.036. PubMed DOI
Gallardo-Ruiz R, Crespo-Facorro B, Setién-Suero E, Tordesillas-Gutierrez D. Long-term Grey Matter changes in First Episode Psychosis: a systematic review. Psychiatry Investig. 2019;16(5):336–45. doi: 10.30773/pi.2019.02.10.1. PubMed DOI PMC
Sayo A, Jennings RG, Van Horn JD. Study factors influencing ventricular enlargement in schizophrenia: a 20 year follow-up meta-analysis. NeuroImage. 2012;59(1):154–67. doi: 10.1016/j.neuroimage.2011.07.011. PubMed DOI PMC
Saijo T, Abe T, Someya Y, Sassa T, Sudo Y, Suhara T, Shuno T, Asai K, Okubo Y. Ten year progressive ventricular enlargement in schizophrenia: an MRI morphometrical study. Psychiatry Clin Neurosci. 2001;55(1):41–7. doi: 10.1046/j.1440-1819.2001.00783.x. PubMed DOI
Gaser C, Nenadic I, Buchsbaum BR, Hazlett EA, Buchsbaum MS. Ventricular enlargement in schizophrenia related to volume reduction of the thalamus, striatum, and superior temporal cortex. Am J Psychiatry. 2004;161(1):154–6. doi: 10.1176/appi.ajp.161.1.154. PubMed DOI
Andreasen NC, Nopoulos P, Magnotta V, Pierson R, Ziebell S, Ho BC. Progressive brain change in schizophrenia: a prospective longitudinal study of first-episode schizophrenia. Biol Psychiatry. 2011;70(7):672–9. doi: 10.1016/j.biopsych.2011.05.017. PubMed DOI PMC
Vita A, De Peri L, Deste G, Sacchetti E. Progressive loss of cortical gray matter in schizophrenia: a meta-analysis and meta-regression of longitudinal MRI studies. Transl Psychiatry. 2012;2(11):e190. doi: 10.1038/tp.2012.116. PubMed DOI PMC
Lieberman J, Chakos M, Wu H, Alvir J, Hoffman E, Robinson D, Bilder R. Longitudinal study of brain morphology in first episode schizophrenia. Biol Psychiatry. 2001;49(6):487–99. doi: 10.1016/S0006-3223(01)01067-8. PubMed DOI
Nakamura M, Salisbury DF, Hirayasu Y, Bouix S, Pohl KM, Yoshida T, Koo MS, Shenton ME, McCarley RW. Neocortical gray matter volume in first-episode schizophrenia and first-episode affective psychosis: a cross-sectional and longitudinal MRI study. Biol Psychiatry. 2007;62(7):773–83. doi: 10.1016/j.biopsych.2007.03.030. PubMed DOI PMC
De Peri L, Crescini A, Deste G, Fusar-Poli P, Sacchetti E, Vita A. Brain structural abnormalities at the onset of schizophrenia and bipolar disorder: a meta-analysis of controlled magnetic resonance imaging studies. Curr Pharm Des. 2012;18(4):486–94. doi: 10.2174/138161212799316253. PubMed DOI
Steen RG, Mull C, McClure R, Hamer RM, Lieberman JA. Brain volume in first-episode schizophrenia: systematic review and meta-analysis of magnetic resonance imaging studies. Br J Psychiatry. 2006;188:510–8. doi: 10.1192/bjp.188.6.510. PubMed DOI
Berger GE, Bartholomeusz CF, Wood SJ, Ang A, Phillips LJ, Proffitt T, Brewer WJ, Smith DJ, Nelson B, Lin A, Borgwardt S, Velakoulis D, Yung AR, McGorry PD, Pantelis C. Ventricular volumes across stages of schizophrenia and other psychoses. Aust N Z J Psychiatry. 2017;51(10):1041–51. doi: 10.1177/0004867417715914. PubMed DOI
Crow TJ. The two-syndrome concept: origins and current status. Schizophr Bull. 1985;11(3):471–86. doi: 10.1093/schbul/11.3.471. PubMed DOI
Andreasen NC, Olsen SA, Dennert JW, Smith MR. Ventricular enlargement in schizophrenia: relationship to positive and negative symptoms. Am J Psychiatry. 1982;139(3):297–302. doi: 10.1176/ajp.139.3.297. PubMed DOI
Klausner JD, Sweeney JA, Deck MD, Haas GL, Kelly AB. Clinical correlates of cerebral ventricular enlargement in schizophrenia. Further evidence for frontal lobe disease. J Nerv Ment Dis. 1992;180(7):407–12. doi: 10.1097/00005053-199207000-00001. PubMed DOI
Garver DL, Nair TR, Christensen JD, Holcomb JA, Kingsbury SJ. Brain and ventricle instability during psychotic episodes of the schizophrenias. Schizophr Res. 2000;44(1):11–23. doi: 10.1016/S0920-9964(00)00015-3. PubMed DOI
Davis KL, Buchsbaum MS, Shihabuddin L, Spiegel-Cohen J, Metzger M, Frecska E, Keefe RS, Powchik P. Ventricular enlargement in poor-outcome schizophrenia. Biol Psychiatry. 1998;43(11):783–93. doi: 10.1016/S0006-3223(97)00553-2. PubMed DOI
Wobrock T, Gruber O, Schneider-Axmann T, Wölwer W, Gaebel W, Riesbeck M, Maier W, Klosterkötter J, Schneider F, Buchkremer G, Möller HJ, Schmitt A, Bender S, Schlösser R, Falkai P. Internal capsule size associated with outcome in first-episode schizophrenia. Eur Arch Psychiatry Clin Neurosci. 2009;259(5):278–83. doi: 10.1007/s00406-008-0867-y. PubMed DOI PMC
Akudjedu TN, Tronchin G, McInerney S, Scanlon C, Kenney JPM, McFarland J, Barker GJ, McCarthy P, Cannon DM, McDonald C, Hallahan B. Progression of neuroanatomical abnormalities after first-episode of psychosis: a 3-year longitudinal sMRI study. J Psychiatr Res. 2020;130:137–51. doi: 10.1016/j.jpsychires.2020.07.034. PubMed DOI
Nesvåg R, Bergmann Ø, Rimol LM, Lange EH, Haukvik UK, Hartberg CB, Fagerberg T, Söderman E, Jönsson EG, Agartz I. A 5-year follow-up study of brain cortical and subcortical abnormalities in a schizophrenia cohort. Schizophr Res. 2012;142(1–3):209–16. doi: 10.1016/j.schres.2012.10.004. PubMed DOI
Bleuler M, Bleuler R. Dementia praecox oder die Gruppe Der Schizophrenien: Eugen Bleuler. Br J Psychiatry. 1986;149:661–2. doi: 10.1192/bjp.149.5.661. PubMed DOI
Strauss JS, Carpenter WT Jr, Bartko JJ. The diagnosis and understanding of schizophrenia. Part III. Speculations on the processes that underlie schizophrenic symptoms and signs. Schizophr Bull 1974 Winter;(11):61–9. PubMed
Tsuang MT, Lyons MJ, Faraone SV. Heterogeneity of schizophrenia. Conceptual models and analytic strategies. Br J Psychiatry. 1990;156:17–26. doi: 10.1192/bjp.156.1.17. PubMed DOI
Buchanan RW, Carpenter WT. Domains of psychopathology: an approach to the reduction of heterogeneity in schizophrenia. J Nerv Ment Dis. 1994;182(4):193–204. doi: 10.1097/00005053-199404000-00001. PubMed DOI
Spaniel F, Tintera J, Rydlo J, Ibrahim I, Kasparek T, Horacek J, Zaytseva Y, Matejka M, Fialova M, Slovakova A, Mikolas P, Melicher T, Görnerova N, Höschl C, Hajek T. Altered neural correlate of the self-agency experience in First-Episode Schizophrenia-Spectrum patients: an fMRI study. Schizophr Bull. 2016;42(4):916–25. doi: 10.1093/schbul/sbv188. PubMed DOI PMC
Sheehan DV, Lecrubier Y, Sheehan KH, Amorim P, Janavs J, Weiller E, Hergueta T, Baker R, Dunbar GC. The mini-international neuropsychiatric interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry. 1998;59(Suppl 20):22–quiz3334. PubMed
Kay SR, Fiszbein A, Opler LA. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull. 1987;13(2):261–76. doi: 10.1093/schbul/13.2.261. PubMed DOI
Aas IH. Global Assessment of Functioning (GAF): properties and frontier of current knowledge. Ann Gen Psychiatry. 2010;9:20. doi: 10.1186/1744-859X-9-20. PubMed DOI PMC
Fischl B. FreeSurfer Neuroimage. 2012;62(2):774–81. doi: 10.1016/j.neuroimage.2012.01.021. PubMed DOI PMC
Reuter M, Schmansky NJ, Rosas HD, Fischl B. Within-subject template estimation for unbiased longitudinal image analysis. NeuroImage. 2012;61(4):1402–18. doi: 10.1016/j.neuroimage.2012.02.084. PubMed DOI PMC
Kempton MJ, Underwood TS, Brunton S, Stylios F, Schmechtig A, Ettinger U, Smith MS, Lovestone S, Crum WR, Frangou S, Williams SC, Simmons A. A comprehensive testing protocol for MRI neuroanatomical segmentation techniques: evaluation of a novel lateral ventricle segmentation method. NeuroImage. 2011;58(4):1051–9. doi: 10.1016/j.neuroimage.2011.06.080. PubMed DOI PMC
Holm S. A simple sequentially rejective multiple Test Procedure. Scand J Stat. 1979;6(2):65–70.
Lindstrom ML, Bates DM. Nonlinear mixed effects models for repeated measures data. Biometrics. 1990;46(3):673–87. doi: 10.2307/2532087. PubMed DOI
Team RDC. A language and environment for statistical computing. 2019 http://wwwR-project.org.
McWhinney SR, Brosch K, Calhoun VD, Crespo-Facorro B, Crossley NA, Dannlowski U, Dickie E, Dietze LMF, Donohoe G, Du Plessis S, Ehrlich S, Emsley R, Furstova P, Glahn DC, Gonzalez-Valderrama A, Grotegerd D, Holleran L, Kircher TTJ, Knytl P, Kolenic M, Lencer R, Nenadić I, Opel N, Pfarr JK, Rodrigue AL, Rootes-Murdy K, Ross AJ, Sim K, Škoch A, Spaniel F, Stein F, Švancer P, Tordesillas-Gutiérrez D, Undurraga J, Vázquez-Bourgon J, Voineskos A, Walton E, Weickert TW, Weickert CS, Thompson PM, van Erp TGM, Turner JA, Hajek T. Correction: obesity and brain structure in schizophrenia - ENIGMA study in 3021 individuals. Mol Psychiatry. 2022;27(9):3738. doi: 10.1038/s41380-022-01696-3. PubMed DOI PMC
Svancer P, Spaniel F. Brain ventricular volume changes in schizophrenia. A narrative review. Neurosci Lett. 2021;759:136065. doi: 10.1016/j.neulet.2021.136065. PubMed DOI
Thompson PM, Hayashi KM, De Zubicaray GI, Janke AL, Rose SE, Semple J, Hong MS, Herman DH, Gravano D, Doddrell DM, Toga AW. Mapping hippocampal and ventricular change in Alzheimer disease. NeuroImage. 2004;22(4):1754–66. doi: 10.1016/j.neuroimage.2004.03.040. PubMed DOI
Puri BK, Hutton SB, Saeed N, Oatridge A, Hajnal JV, Duncan L, Chapman MJ, Barnes TR, Bydder GM, Joyce EM. A serial longitudinal quantitative MRI study of cerebral changes in first-episode schizophrenia using image segmentation and subvoxel registration. Psychiatry Res. 2001;106(2):141–50. doi: 10.1016/S0925-4927(01)00072-5. PubMed DOI
DeLisi LE, Stritzke P, Riordan H, Holan V, Boccio A, Kushner M, McClelland J, Van Eyl O, Anand A. The timing of brain morphological changes in schizophrenia and their relationship to clinical outcome. Biol Psychiatry. 1992;31(3):241–54. doi: 10.1016/0006-3223(92)90047-4. PubMed DOI
Williams AO, Reveley MA, Kolakowska T, Ardern M, Mandelbrote BM. Schizophrenia with good and poor outcome. II: cerebral ventricular size and its clinical significance. Br J Psychiatry. 1985;146:239–46. doi: 10.1192/bjp.146.3.239. PubMed DOI
Arango C, Rapado-Castro M, Reig S, Castro-Fornieles J, González-Pinto A, Otero S, Baeza I, Moreno C, Graell M, Janssen J, Parellada M, Moreno D, Bargalló N, Desco M. Progressive brain changes in children and adolescents with first-episode psychosis. Arch Gen Psychiatry. 2012;69(1):16–26. doi: 10.1001/archgenpsychiatry.2011.150. PubMed DOI
Heilbronner U, Samara M, Leucht S, Falkai P, Schulze TG. The longitudinal course of Schizophrenia across the Lifespan: clinical, cognitive, and neurobiological aspects. Harv Rev Psychiatry. 2016 Mar-Apr;24(2):118–28. PubMed PMC
Jauhar S, Johnstone M, McKenna PJ. Schizophrenia Lancet. 2022;399(10323):473–86. doi: 10.1016/S0140-6736(21)01730-X. PubMed DOI
Vojinovic D, Adams HH, Jian X, Yang Q, Smith AV, Bis JC, Teumer A, Scholz M, Armstrong NJ, Hofer E, Saba Y, Luciano M, Bernard M, Trompet S, Yang J, Gillespie NA, van der Lee SJ, Neumann A, Ahmad S, Andreassen OA, Ames D, Amin N, Arfanakis K, Bastin ME, Becker DM, Beiser AS, Beyer F, Brodaty H, Bryan RN, Bülow R, Dale AM, De Jager PL, Deary IJ, DeCarli C, Fleischman DA, Gottesman RF, van der Grond J, Gudnason V, Harris TB, Homuth G, Knopman DS, Kwok JB, Lewis CE, Li S, Loeffler M, Lopez OL, Maillard P, El Marroun H, Mather KA, Mosley TH, Muetzel RL, Nauck M, Nyquist PA, Panizzon MS, Pausova Z, Psaty BM, Rice K, Rotter JI, Royle N, Satizabal CL, Schmidt R, Schofield PR, Schreiner PJ, Sidney S, Stott DJ, Thalamuthu A, Uitterlinden AG, Valdés Hernández MC, Vernooij MW, Wen W, White T, Witte AV, Wittfeld K, Wright MJ, Yanek LR, Tiemeier H, Kremen WS, Bennett DA, Jukema JW, Paus T, Wardlaw JM, Schmidt H, Sachdev PS, Villringer A, Grabe HJ, Longstreth WT, van Duijn CM, Launer LJ, Seshadri S, Ikram MA, Fornage M. Genome-wide association study of 23,500 individuals identifies 7 loci associated with brain ventricular volume. Nat Commun. 2018;9(1):3945. doi: 10.1038/s41467-018-06234-w. PubMed DOI PMC
Mokri B. The Monro-Kellie hypothesis: applications in CSF volume depletion. Neurology. 2001;56(12):1746–8. doi: 10.1212/WNL.56.12.1746. PubMed DOI
Valova G, Bogomyakova O, Tulupov A, Cherevko A. Influence of interaction of cerebral fluids on ventricular deformation: a mathematical approach. PLoS ONE. 2022;17(2):e0264395. doi: 10.1371/journal.pone.0264395. PubMed DOI PMC
Doron O, Zadka Y, Barnea O, Rosenthal G. Interactions of brain, blood, and CSF: a novel mathematical model of cerebral edema. Fluids Barriers CNS. 2021;18(1):42. doi: 10.1186/s12987-021-00274-z. PubMed DOI PMC
Fraguas D, Díaz-Caneja CM, Ayora M, Hernández-Álvarez F, Rodríguez-Quiroga A, Recio S, Leza JC, Arango C. Oxidative stress and inflammation in first-episode psychosis: a systematic review and Meta-analysis. Schizophr Bull. 2019;45(4):742–51. doi: 10.1093/schbul/sby125. PubMed DOI PMC
Stamatovic SM, Dimitrijevic OB, Keep RF, Andjelkovic AV. Inflammation and brain edema: new insights into the role of chemokines and their receptors. Acta Neurochir Suppl. 2006;96:444–50. doi: 10.1007/3-211-30714-1_91. PubMed DOI
Michinaga S, Koyama Y. Pathogenesis of brain edema and investigation into anti-edema drugs. Int J Mol Sci. 2015;16(5):9949–75. doi: 10.3390/ijms16059949. PubMed DOI PMC
Hoang D, Xu Y, Lutz O, Bannai D, Zeng V, Bishop JR, Keshavan M, Lizano P. Inflammatory subtypes in Antipsychotic-Naïve First-Episode Schizophrenia are Associated with altered brain morphology and Topological Organization. Brain Behav Immun. 2022;100:297–308. doi: 10.1016/j.bbi.2021.11.019. PubMed DOI PMC
Lizano P, Lutz O, Xu Y, Rubin LH, Paskowitz L, Lee AM, Eum S, Keedy SK, Hill SK, Reilly JL, Wu B, Tamminga CA, Clementz BA, Pearlson GD, Gershon ES, Keshavan MS, Sweeney JA, Bishop JR. Multivariate relationships between peripheral inflammatory marker subtypes and cognitive and brain structural measures in psychosis. Mol Psychiatry. 2021;26(7):3430–43. doi: 10.1038/s41380-020-00914-0. PubMed DOI PMC
Bergé D, Mané A, Lesh TA, Bioque M, Barcones F, Gonzalez-Pinto AM, Parellada M, Vieta E, Castro-Fornieles J, Rodriguez-Jimenez R, García-Portilla MP, Usall J, Carter CS, Cabrera B, Bernardo M, Janssen J. PEPs group (collaborators). Elevated Extracellular Free-Water in a Multicentric First-Episode psychosis sample, decrease during the First 2 years of illness. Schizophr Bull. 2020;46(4):846–56. doi: 10.1093/schbul/sbz132. PubMed DOI PMC
Fitzsimmons J, Schneiderman JS, Whitford TJ, Swisher T, Niznikiewicz MA, Pelavin PE, Terry DP, Mesholam-Gately RI, Seidman LJ, Goldstein JM, Kubicki M. Cingulum bundle diffusivity and delusions of reference in first episode and chronic schizophrenia. Psychiatry Res. 2014;224(2):124–32. doi: 10.1016/j.pscychresns.2014.08.002. PubMed DOI PMC
Montal V, Vilaplana E, Alcolea D, Pegueroles J, Pasternak O, González-Ortiz S, Clarimón J, Carmona-Iragui M, Illán-Gala I, Morenas-Rodríguez E, Ribosa-Nogué R, Sala I, Sánchez-Saudinós MB, García-Sebastian M, Villanúa J, Izagirre A, Estanga A, Ecay-Torres M, Iriondo A, Clerigue M, Tainta M, Pozueta A, González A, Martínez-Heras E, Llufriu S, Blesa R, Sanchez-Juan P, Martínez-Lage P, Lleó A, Fortea J. Cortical microstructural changes along the Alzheimer’s disease continuum. Alzheimers Dement. 2018;14(3):340–51. doi: 10.1016/j.jalz.2017.09.013. PubMed DOI
Moscarelli M. A major flaw in the diagnosis of schizophrenia: what happened to the Schneider’s first rank symptoms. Psychol Med. 2020;50(9):1409–17. doi: 10.1017/S0033291720001816. PubMed DOI