Characterization of the extracellular free water signal in schizophrenia using multi-site diffusion MRI harmonization.
Journal
Molecular psychiatry
ISSN: 1476-5578
Titre abrégé: Mol Psychiatry
Pays: England
ID NLM: 9607835
Informations de publication
Date de publication:
May 2023
May 2023
Historique:
received:
09
06
2022
accepted:
05
04
2023
revised:
06
03
2023
pubmed:
25
4
2023
medline:
25
4
2023
entrez:
24
04
2023
Statut:
ppublish
Résumé
Studies applying Free Water Imaging have consistently reported significant global increases in extracellular free water (FW) in populations of individuals with early psychosis. However, these published studies focused on homogenous clinical participant groups (e.g., only first episode or chronic), thereby limiting our understanding of the time course of free water elevations across illness stages. Moreover, the relationship between FW and duration of illness has yet to be directly tested. Leveraging our multi-site diffusion magnetic resonance imaging(dMRI) harmonization approach, we analyzed dMRI scans collected by 12 international sites from 441 healthy controls and 434 individuals diagnosed with schizophrenia-spectrum disorders at different illness stages and ages (15-58 years). We characterized the pattern of age-related FW changes by assessing whole brain white matter in individuals with schizophrenia and healthy controls. In individuals with schizophrenia, average whole brain FW was higher than in controls across all ages, with the greatest FW values observed from 15 to 23 years (effect size range = [0.70-0.87]). Following this peak, FW exhibited a monotonic decrease until reaching a minima at the age of 39 years. After 39 years, an attenuated monotonic increase in FW was observed, but with markedly smaller effect sizes when compared to younger patients (effect size range = [0.32-0.43]). Importantly, FW was found to be negatively associated with duration of illness in schizophrenia (p = 0.006), independent of the effects of other clinical and demographic data. In summary, our study finds in a large, age-diverse sample that participants with schizophrenia with a shorter duration of illness showed higher FW values compared to participants with more prolonged illness. Our findings provide further evidence that elevations in the FW are present in individuals with schizophrenia, with the greatest differences in the FW being observed in those at the early stages of the disorder, which might suggest acute extracellular processes.
Identifiants
pubmed: 37095352
doi: 10.1038/s41380-023-02068-1
pii: 10.1038/s41380-023-02068-1
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2030-2038Subventions
Organisme : Medical Research Council
ID : G0500092
Pays : United Kingdom
Organisme : NIMH NIH HHS
ID : K01 MH115247
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH130781
Pays : United States
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Kelly S, Jahanshad N, Zalesky A, Kochunov P, Agartz I, Alloza C, et al. Widespread white matter microstructural differences in schizophrenia across 4322 individuals: results from the ENIGMA Schizophrenia DTI Working Group. Mol Psychiatry. 2017;23:1261–9.
pubmed: 29038599
pmcid: 5984078
doi: 10.1038/mp.2017.170
Kubicki M, McCarley R, Westin C-F, Park H-J, Maier S, Kikinis R, et al. A review of diffusion tensor imaging studies in schizophrenia. J Psychiatr Res. 2007;41:15–30.
pubmed: 16023676
doi: 10.1016/j.jpsychires.2005.05.005
Wheeler AL, Voineskos AN. A review of structural neuroimaging in schizophrenia: from connectivity to connectomics. Front Hum Neurosci. 2014;8:653.
pubmed: 25202257
pmcid: 4142355
doi: 10.3389/fnhum.2014.00653
Holleran L, Kelly S, Alloza C, Agartz I, Andreassen OA, Arango C, et al. The relationship between white matter microstructure and general cognitive ability in patients with schizophrenia and healthy participants in the ENIGMA Consortium. Am J Psychiatry. 2020;177:537–47.
pubmed: 32212855
pmcid: 7938666
doi: 10.1176/appi.ajp.2019.19030225
Cetin-Karayumak S, Biase MAD, Chunga N, Reid B, Somes N, Lyall AE, et al. White matter abnormalities across the lifespan of schizophrenia: a harmonized multi-site diffusion MRI study. Mol Psychiatry. 2019;25:3208–19.
pubmed: 31511636
pmcid: 7147982
doi: 10.1038/s41380-019-0509-y
O’Donnell LJ, Pasternak O. Does diffusion MRI tell us anything about the white matter? An overview of methods and pitfalls. Schizophr Res. 2015;161:133–41.
pubmed: 25278106
doi: 10.1016/j.schres.2014.09.007
Jones DK, Knösche TR, Turner R. White matter integrity, fiber count, and other fallacies: the do’s and don’ts of diffusion MRI. NeuroImage. 2013;73:239–54.
pubmed: 22846632
doi: 10.1016/j.neuroimage.2012.06.081
Pasternak O, Sochen N, Gur Y, Intrator N, Assaf Y. Free water elimination and mapping from diffusion MRI. Magn Reson Med. 2009;62:717–30.
pubmed: 19623619
doi: 10.1002/mrm.22055
Pasternak O, Westin C-F, Bouix S, Seidman LJ, Goldstein JM, Woo T-UW, et al. Excessive extracellular volume reveals a neurodegenerative pattern in schizophrenia onset. J Neurosci. 2012;32:17365–72.
pubmed: 23197727
pmcid: 3549332
doi: 10.1523/JNEUROSCI.2904-12.2012
Lyall AE, Pasternak O, Robinson DG, Newell D, Trampush JW, Gallego JA, et al. Greater extracellular free-water in first-episode psychosis predicts better neurocognitive functioning. Mol Psychiatry. 2018;23:701–7.
pubmed: 28348381
doi: 10.1038/mp.2017.43
Lesh TA, Maddock RJ, Howell A, Wang H, Tanase C, Daniel Ragland J, et al. Extracellular free water and glutathione in first-episode psychosis-a multimodal investigation of an inflammatory model for psychosis. Mol Psychiatry. 2021;26:761–71.
Bergé D, Mané A, Lesh TA, Bioque M, Barcones F, Gonzalez-Pinto AM, et al. Elevated extracellular free-water in a multicentric first-episode psychosis sample, decrease during the first 2 years of illness. Schizophr Bull 2020;46:846–56.
pubmed: 31915835
pmcid: 7342177
doi: 10.1093/schbul/sbz132
Guo JY, Lesh TA, Niendam TA, Ragland JD, Tully LM, Carter CS. Brain free water alterations in first-episode psychosis: a longitudinal analysis of diagnosis, course of illness, and medication effects. Psychol Med. 2020;45:1–10.
Pasternak O, Westin CF, Dahlben B, Bouix S, Kubicki M. The extent of diffusion MRI markers of neuroinflammation and white matter deterioration in chronic schizophrenia. Schizophr Res. 2015;161:113–8.
Oestreich LKL, Lyall AE, Pasternak O, Kikinis Z, Newell DT, Savadjiev P, et al. Characterizing white matter changes in chronic schizophrenia: a free-water imaging multi-site study. Schizophr Res. 2017;189:153–61.
pubmed: 28190639
pmcid: 5552442
doi: 10.1016/j.schres.2017.02.006
Gurholt TP, Haukvik UK, Lonning V, Jönsson EG, Pasternak O, Agartz I. Microstructural white matter and links with subcortical structures in chronic schizophrenia: a free-water imaging approach. Front Psychiatry. 2020;11:56.
pubmed: 32180735
pmcid: 7057718
doi: 10.3389/fpsyt.2020.00056
Mandl RCW, Pasternak O, Cahn W, Kubicki M, Kahn RS, Shenton ME, et al. Comparing free water imaging and magnetization transfer measurements in schizophrenia. Schizophr Res. 2015;161:126–32.
pubmed: 25454797
doi: 10.1016/j.schres.2014.09.046
Chang X, Mandl RCW, Pasternak O, Brouwer RM, Cahn W, Collin G, et al. Diffusion MRI derived free-water imaging measures in patients with schizophrenia and their non-psychotic siblings. Prog Neuro-Psychopharmacol Biol Psychiatry. 2021;109:110238.
doi: 10.1016/j.pnpbp.2020.110238
Karayumak SC, Bouix S, Ning L, James A, Crow T, Shenton M, et al. Retrospective harmonization of multi-site diffusion MRI data acquired with different acquisition parameters. NeuroImage. 2019;184:180–200.
doi: 10.1016/j.neuroimage.2018.08.073
Seitz-Holland J, Cetin-Karayumak S, Wojcik JD, Lyall A, Levitt J, Shenton ME, et al. Elucidating the relationship between white matter structure, demographic, and clinical variables in schizophrenia—a multicenter harmonized diffusion tensor imaging study. Mol Psychiatry. 2021;26:5357–70.
Elad D, Cetin‐Karayumak S, Zhang F, Cho KIK, Lyall AE, Seitz‐Holland J, et al. Improving the predictive potential of diffusion MRI in schizophrenia using normative models—towards subject‐level classification. Hum Brain Mapp. 2021;42:4658–70.
pubmed: 34322947
pmcid: 8410550
doi: 10.1002/hbm.25574
Seitz J, Cetin-Karayumak S, Lyall A, Pasternak O, Baxi M, Vangel M, et al. Investigating sexual dimorphism of human white matter in a harmonized, multi-site diffusion magnetic resonance imaging study. Cereb Cortex. 2020;31:201–12.
pmcid: 7727358
doi: 10.1093/cercor/bhaa220
Biase MAD, Zalesky A, Cetin-Karayumak S, Rathi Y, Lv J, Boerrigter D, et al. Large-scale evidence for an association between peripheral inflammation and white matter free water in schizophrenia and healthy individuals. Schizophr Bull. 2020. https://doi.org/10.1093/schbul/sbaa134 .
Ye H, Zalesky A, Lv J, Loi SM, Cetin-Karayumak S, Rathi Y, et al. Network analysis of symptom comorbidity in schizophrenia: relationship to illness course and brain white matter microstructure. Schizophr Bull. 2021. https://doi.org/10.1093/schbul/sbab015 .
Kelly S, Guimond S, Pasternak O, Lutz O, Lizano P, Cetin-Karayumak S, et al. White matter microstructure across brain-based biotypes for psychosis—findings from the bipolar-schizophrenia network for intermediate phenotypes. Psychiatry Res Neuroimaging. 2021;308:111234.
pubmed: 33385763
doi: 10.1016/j.pscychresns.2020.111234
Di Biase MA, Cetin-Karayumak S, Lyall AE, Zalesky A, Cho KIK, Zhang F, et al. White matter changes in psychosis risk relate to development and are not impacted by the transition to psychosis. Mol Psychiatry. 2021;26:6833–44.
Andersson JLR, Sotiropoulos SN. An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging. Neuroimage. 2016;125:1063–78.
pubmed: 26481672
doi: 10.1016/j.neuroimage.2015.10.019
Smith SM. Fast robust automated brain extraction. Hum Brain Mapp. 2002;17:143–55.
pubmed: 12391568
pmcid: 6871816
doi: 10.1002/hbm.10062
Ning L, Bonet-Carne E, Grussu F, Sepehrband F, Kaden E, Veraart J, et al. Cross-scanner and cross-protocol multi-shell diffusion MRI data harmonization: algorithms and results. Neuroimage. 2020;221:117128.
pubmed: 32673745
doi: 10.1016/j.neuroimage.2020.117128
Varentsova A, Zhang S, Arfanakis K. Development of a high angular resolution diffusion imaging human brain template. Neuroimage. 2014;91:177–86.
pubmed: 24440528
doi: 10.1016/j.neuroimage.2014.01.009
Cetin Karayumak S, Kubicki M, Rathi Y. Harmonizing Diffusion MRI Data Across Magnetic Field Strengths. In: Frangi A, Schnabel J, Davatzikos C, Alberola-López C, Fichtinger G, editors. Medical Image Computing and Computer Assisted Intervention – MICCAI 2018. MICCAI 2018. Lecture Notes in Computer Science, vol. 11072. Springer, Cham; 2018.
Kailath T. The divergence and Bhattacharyya distance measures in signal selection. IEEE Trans Commun Technol. 1967;15:52–60.
doi: 10.1109/TCOM.1967.1089532
Cropley VL, Klauser P, Lenroot RK, Bruggemann J, Sundram S, Bousman C, et al. Accelerated gray and white matter deterioration with age in schizophrenia. Am J Psychiatry. 2017;174:286–95.
pubmed: 27919183
doi: 10.1176/appi.ajp.2016.16050610
Carreira Figueiredo I, Borgan F, Pasternak O, Turkheimer FE, Howes OD. White-matter free-water diffusion MRI in schizophrenia: a systematic review and meta-analysis. Neuropsychopharmacology. 2022;47:1413–20.
Fusar‐Poli P, McGorry PD, Kane JM. Improving outcomes of first‐episode psychosis: an overview. World Psychiatry. 2017;16:251–65.
pubmed: 28941089
pmcid: 5608829
doi: 10.1002/wps.20446
Robinson DG, Schooler NR, Rosenheck RA, Lin H, Sint KJ, Marcy P, et al. Predictors of hospitalization of individuals with first-episode psychosis: data from a 2-year follow-up of the RAISE-ETP. Psychiatr Serv. 2019;70:569–77.
pubmed: 31084291
pmcid: 6602852
doi: 10.1176/appi.ps.201800511
Biase MAD, Katabi G, Piontkewitz Y, Karayumak SC, Weiner I, Pasternak O. Increased extracellular free-water in adult male rats following in utero exposure to maternal immune activation. Brain Behav Immun. 2019. https://doi.org/10.1016/j.bbi.2019.09.010 .
Piontkewitz Y, Arad M, Weiner I. Abnormal trajectories of neurodevelopment and behavior following in utero insult in the rat. Biol Psychiatry. 2011;70:842–51.
pubmed: 21816387
doi: 10.1016/j.biopsych.2011.06.007
Gallego JA, Blanco EA, Husain-Krautter S, Fagen EM, Moreno-Merino P, del Ojo-Jiménez JA, et al. Cytokines in cerebrospinal fluid of patients with schizophrenia spectrum disorders: new data and an updated meta-analysis. Schizophr Res. 2018. https://doi.org/10.1016/j.schres.2018.07.019 .
Coughlin JM, Wang Y, Ambinder EB, Ward RE, Minn I, Vranesic M, et al. In vivo markers of inflammatory response in recent-onset schizophrenia: a combined study using |[lsqb]|11C|[rsqb]|DPA-713 PET and analysis of CSF and plasma. Transl Psychiatry. 2016;6:e777.
pubmed: 27070405
pmcid: 4872398
doi: 10.1038/tp.2016.40
Söderlund J, Schröder J, Nordin C, Samuelsson M, Walther-Jallow L, Karlsson H, et al. Activation of brain interleukin-1beta in schizophrenia. Mol Psychiatry. 2009;14:1069–71.
pubmed: 19920835
pmcid: 2848473
doi: 10.1038/mp.2009.52
Pakkenberg B. Total nerve cell number in neocortex in chronic schizophrenics and controls estimated using optical disectors. Biol Psychiatry. 1993;34:768–72.
pubmed: 8292680
doi: 10.1016/0006-3223(93)90065-L
Pakkenberg B. The volume of the mediodorsal thalamic nucleus in treated and untreated schizophrenics. Schizophr Res. 1992;7:95–100.
pubmed: 1355358
doi: 10.1016/0920-9964(92)90038-7
Pakkenberg B. Pronounced reduction of total neuron number in mediodorsal thalamic nucleus and nucleus accumbens in schizophrenics. Arch Gen Psychiatry. 1990;47:1023–8.
pubmed: 2241504
doi: 10.1001/archpsyc.1990.01810230039007
Angoff R, Himali JJ, Maillard P, Aparicio HJ, Vasan RS, Seshadri S, et al. Relations of metabolic health and obesity to brain aging in young to middle‐aged adults. J Am Heart Assoc. 2021;11:e022107.
doi: 10.1161/JAHA.121.022107
Andreasen NC, Nopoulos P, Magnotta V, Pierson R, Ziebell S, Ho B-C. Progressive brain change in schizophrenia: a prospective longitudinal study of first-episode schizophrenia. Biol Psychiatry. 2011;70:672–9.
pubmed: 21784414
pmcid: 3496792
doi: 10.1016/j.biopsych.2011.05.017
Fusar-Poli P, Smieskova R, Kempton MJ, Ho B-C, Andreasen NC, Borgwardt S. Progressive brain changes in schizophrenia related to antipsychotic treatment? A meta-analysis of longitudinal MRI studies. Neurosci Biobehav Rev. 2013;37:1680–91.
pubmed: 23769814
pmcid: 3964856
doi: 10.1016/j.neubiorev.2013.06.001
Gao X, Zhang W, Yao L, Xiao Y, Liu L, Liu J, et al. Association between structural and functional brain alterations in drug-free patients with schizophrenia: a multimodal meta-analysis. J Psychiatry Neurosci Jpn. 2018;43:131–42.
pubmed: 29481320
doi: 10.1503/jpn.160219
Tuozzo C, Lyall AE, Pasternak O, James ACD, Crow TJ, Kubicki M. Patients with chronic bipolar disorder exhibit widespread increases in extracellular free water. Bipolar Disord. 2018;20:523–30.
pubmed: 29227016
doi: 10.1111/bdi.12588
Seitz-Holland J, Nägele FL, Kubicki M, Pasternak O, Cho KIK, Hough M, et al. Shared and distinct white matter abnormalities in adolescent-onset schizophrenia and adolescent-onset psychotic bipolar disorder. Psychol Med. 2022:1–13. https://doi.org/10.1017/S003329172200160X .
Langhein M, Seitz-Holland J, Lyall AE, Pasternak O, Chunga N, Cetin-Karayumak S, et al. Association between peripheral inflammation and free-water imaging in major depressive disorder before and after ketamine treatment—a pilot study. J Affect Disord. 2022;314:78–85.
pubmed: 35779673
doi: 10.1016/j.jad.2022.06.043
Maziero MP, Seitz-Holland J, Cho KIK, Goldenberg JE, Tanamatis TW, Diniz JB, et al. Cellular and extracellular white matter abnormalities in obsessive-compulsive disorder: a diffusion magnetic resonance imaging study. Biol Psychiatry Cogn Neurosci Neuroimaging. 2021;6:983–91.
pubmed: 33862255
pmcid: 8502196
Garcia TP, Marder K. Statistical approaches to longitudinal data analysis in neurodegenerative diseases: Huntington’s disease as a model. Curr Neurol Neurosci. 2017;17:14.
doi: 10.1007/s11910-017-0723-4
Aghili M, Tabarestani S, Adjouadi M. Addressing the missing data challenge in multi-modal datasets for the diagnosis of Alzheimer’s disease. J Neurosci Methods. 2022;375:109582.
Rydhög AS, Szczepankiewicz F, Wirestam R, Ahlgren A, Westin C-F, Knutsson L, et al. Separating blood and water: perfusion and free water elimination from diffusion MRI in the human brain. Neuroimage. 2017;156:423–34.
pubmed: 28412443
doi: 10.1016/j.neuroimage.2017.04.023
Berger M, Pirpamer L, Hofer E, Ropele S, Duering M, Gesierich B, et al. Free water diffusion MRI and executive function with a speed component in healthy aging. Neuroimage. 2022;257:119303.
pubmed: 35568345
doi: 10.1016/j.neuroimage.2022.119303
Kubicki M, Lyall AE. Antipsychotics and their impact on cerebral white matter: part of the problem or part of the solution? Am J Psychiatry. 2018;175:1056–7.
pubmed: 30380938
doi: 10.1176/appi.ajp.2018.18060752
Karcher NR, Barch DM. The ABCD study: understanding the development of risk for mental and physical health outcomes. Neuropsychopharmacology. 2021;46:131–42.
pubmed: 32541809
doi: 10.1038/s41386-020-0736-6
Elam JS, Glasser MF, Harms MP, Sotiropoulos SN, Andersson JLR, Burgess GC, et al. The Human Connectome Project: a retrospective. Neuroimage. 2021;244:118543.
pubmed: 34508893
doi: 10.1016/j.neuroimage.2021.118543
Seidman LJ, Shapiro DI, Stone WS, Woodberry KA, Ronzio A, Cornblatt BA, et al. Association of neurocognition with transition to psychosis: baseline functioning in the second phase of the North American Prodrome Longitudinal Study. JAMA Psychiatry. 2016;73:1239–1248.
pubmed: 27806157
pmcid: 5511703
doi: 10.1001/jamapsychiatry.2016.2479
Chung Y, Cannon TD. Brain imaging during the transition from psychosis prodrome to schizophrenia. J Nerv Ment Dis. 2015;203:336–341.
pubmed: 25900551
pmcid: 4414922
doi: 10.1097/NMD.0000000000000286
Johnstone EC, Abukmeil SS, Byrne M, Clafferty R, Grant E, Hodges A, et al. Edinburgh high risk study—findings after four years: demographic, attainment and psychopathological issues. Schizophr Res. 2000;46:1–15.
pubmed: 11099880
doi: 10.1016/S0920-9964(99)00225-X
Pantelis C, Velakoulis D, Wood SJ, Yücel M, Yung AR, Phillips LJ, et al. Neuroimaging and emerging psychotic disorders: the Melbourne ultra-high risk studies. Int Rev Psychiatry. 2007;19:371–81.
pubmed: 17671870
doi: 10.1080/09540260701512079
Addington J, Cadenhead KS, Cornblatt BA, Mathalon DH, McGlashan TH, Perkins DO, et al. North American Prodrome Longitudinal Study (NAPLS 2): overview and recruitment. Schizophr Res. 2012;142:77–82.
pubmed: 23043872
pmcid: 3502644
doi: 10.1016/j.schres.2012.09.012
Yung AR, Nelson B. Young people at ultra high risk for psychosis: research from the PACE clinic. Rev Bras Psiquiatr. 2011;33:s143–60.
pubmed: 22286565
doi: 10.1590/S1516-44462011000600003