Brain ageing in schizophrenia: evidence from 26 international cohorts via the ENIGMA Schizophrenia consortium

. 2023 Mar ; 28 (3) : 1201-1209. [epub] 20221209

Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic

Typ dokumentu metaanalýza, časopisecké články, Research Support, N.I.H., Extramural, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid36494461

Grantová podpora
R01 MH118695 NIMH NIH HHS - United States
R01 NS114628 NINDS NIH HHS - United States
R21 MH097196 NIMH NIH HHS - United States
R01 EB015611 NIBIB NIH HHS - United States
RF1 NS114628 NINDS NIH HHS - United States
R01 MH116147 NIMH NIH HHS - United States
RF1 MH123163 NIMH NIH HHS - United States
U24 RR021992 NCRR NIH HHS - United States
R01 MH121246 NIMH NIH HHS - United States
U24 RR025736 NCRR NIH HHS - United States
R01 AG059874 NIA NIH HHS - United States
R01 MH083968 NIMH NIH HHS - United States
R01 MH121101 NIMH NIH HHS - United States
MR/R024790/1 Medical Research Council - United Kingdom
U54 EB020403 NIBIB NIH HHS - United States
R01 MH117601 NIMH NIH HHS - United States
MR/R024790/2 Medical Research Council - United Kingdom
S10 OD023696 NIH HHS - United States

Odkazy

PubMed 36494461
PubMed Central PMC10005935
DOI 10.1038/s41380-022-01897-w
PII: 10.1038/s41380-022-01897-w
Knihovny.cz E-zdroje

Schizophrenia (SZ) is associated with an increased risk of life-long cognitive impairments, age-related chronic disease, and premature mortality. We investigated evidence for advanced brain ageing in adult SZ patients, and whether this was associated with clinical characteristics in a prospective meta-analytic study conducted by the ENIGMA Schizophrenia Working Group. The study included data from 26 cohorts worldwide, with a total of 2803 SZ patients (mean age 34.2 years; range 18-72 years; 67% male) and 2598 healthy controls (mean age 33.8 years, range 18-73 years, 55% male). Brain-predicted age was individually estimated using a model trained on independent data based on 68 measures of cortical thickness and surface area, 7 subcortical volumes, lateral ventricular volumes and total intracranial volume, all derived from T1-weighted brain magnetic resonance imaging (MRI) scans. Deviations from a healthy brain ageing trajectory were assessed by the difference between brain-predicted age and chronological age (brain-predicted age difference [brain-PAD]). On average, SZ patients showed a higher brain-PAD of +3.55 years (95% CI: 2.91, 4.19; I2 = 57.53%) compared to controls, after adjusting for age, sex and site (Cohen's d = 0.48). Among SZ patients, brain-PAD was not associated with specific clinical characteristics (age of onset, duration of illness, symptom severity, or antipsychotic use and dose). This large-scale collaborative study suggests advanced structural brain ageing in SZ. Longitudinal studies of SZ and a range of mental and somatic health outcomes will help to further evaluate the clinical implications of increased brain-PAD and its ability to be influenced by interventions.

3rd Faculty of Medicine Charles University Prague Czech Republic

Advanced Computation and e Science Instituto de Física de Cantabria CSIC Santander Spain

Campbell Family Mental Health Research Institute CAMH Toronto Canada

Center for the Neurobiology of Learning and Memory University of California Irvine CA USA

Centre for Medical Image Computing Department of Computer Science University College London London UK

Centre for Neuroimaging and Cognitive Genomics School of Psychology National University of Ireland Galway Galway Ireland

Centre for Youth Mental Health The University of Melbourne Melbourne VIC Australia

Centro de Investigación Biomédica en Red de Salud Mental Instituto de Salud Carlos 3 Spain

Clinical Translational Neuroscience Laboratory Department of Psychiatry and Human Behavior University of California Irvine Irvine CA USA

Dementia Research Centre Queen Square Institute of Neurology University College London London UK

Department of Brain and Cognitive Sciences Seoul National University College of Natural Sciences Seoul South Korea

Department of Child and Adolescent Psychiatry Institute of Psychiatry and Mental Health Hospital General Universitario Gregorio Marañón IiSGM CIBERSAM School of Medicine Universidad Complutense Madrid Spain

Department of Computer Science Georgia State University Atlanta GA USA

Department of Experimental Psychopathology and Psychotherapy University of Zurich Zurich Switzerland

Department of Neuroimaging Institute of Psychiatry Psychology and Neuroscience King's College London London UK

Department of Neuropsychiatry Seoul National University Hospital Seoul South Korea

Department of Neuroscience and Physiology SUNY Upstate Medical University Syracuse NY USA

Department of Neurosurgery School of Mental Health and Neuroscience EURON Maastricht University Medical Centre Maastricht The Netherlands

Department of Psychiatry Amsterdam University Medical Centers Vrije Universiteit and GGZ inGeest Amsterdam Neuroscience Amsterdam The Netherlands

Department of Psychiatry and Behavioral Sciences Baylor College of Medicine Houston TX USA

Department of Psychiatry and Human Behavior University of California Irvine CA USA

Department of Psychiatry and Neuropsychology Maastricht University Maastricht The Netherlands

Department of Psychiatry and Psychotherapy Ludwig Maximilians Universität Munich Munich Germany

Department of Psychiatry Jeonbuk National University Hospital Jeonju Korea

Department of Psychiatry Jeonbuk National University Medical School Jeonju Korea

Department of Psychiatry Marqués de Valdecilla University Hospital IDIVAL School of Medicine University of Cantabria Santander Spain

Department of Psychiatry Monash University Clayton VIC Australia

Department of Psychiatry Psychiatric University Hospital University of Basel Basel Switzerland

Department of Psychiatry Psychosomatics and Psychotherapy University of Lübeck Lübeck Germany

Department of Psychiatry Psychotherapy and Psychosomatics Psychiatric Hospital University of Zurich Zurich Switzerland

Department of Psychiatry Seoul National University College of Medicine Seoul South Korea

Department of Psychiatry Stellenbosch University Cape Town South Africa

Department of Psychiatry University of Basel Basel Switzerland

Department of Psychiatry University of California San Diego San Diego CA USA

Department of Psychiatry University of New Mexico Albuquerque NM USA

Department of Psychiatry University of Toronto Toronto ON Canada

Department of Psychology Georgia State University Atlanta GA USA

Department of Psychology School of Arts and Social Sciences City University of London London UK

Department of Psychology School of Business National College of Ireland Dublin Ireland

Department of Psychology University of Bath Bath UK

Department of Radiology Marqués de Valdecilla University Hospital Valdecilla Biomedical Research Institute IDIVAL Santander Spain

Department of Translational Biomedicine and Neuroscience University of Bari Aldo Moro Bari Italy

Desert Pacific Mental Illness Research Education and Clinical Center VA San Diego Healthcare System San Diego CA USA

Division of Addiction Medicine Centre Hospitalier des Quatre Villes St Cloud France

Division of Adult Psychiatry Department of Psychiatry Geneva University Hospitals Geneva Switzerland

Faculty of Electrical Engineering Czech Technical University Prague Prague Czech Republic

FIDMAG Germanes Hospitalàries Research Foundation Barcelona Catalonia Spain

Florey Institute of Neuroscience and Mental Health Parkville VIC Australia

Hospital Benito Menni CASM Sant Boi de Llobregat Catalonia Spain

Hospital Universitario Virgen del Rocío IBiS CSIC Universidad de Sevilla Seville Spain

Hunter Medical Research Institute Newcastle NSW Australia

Imaging Genetics Center Stevens Neuroimaging and Informatics Institute Keck School of Medicine University of Southern California Marina del Rey CA USA

Institute for Translational Psychiatry University of Münster Münster Germany

Institute of Computer Science Czech Academy of Sciences Prague Czech Republic

Laboratory of Neuropsychiatry IRCCS Santa Lucia Foundation Rome Italy

Lee Kong Chian School of Medicine Nanyang Technological University Singapore Singapore

Maryland Psychiatric Research Center Department of Psychiatry University of Maryland School of Medicine Baltimore MD USA

McConnell Brain Imaging Centre Montreal Neurological Institute and Hospital McGill University Montreal QC Canada

Melbourne Neuropsychiatry Centre Department of Psychiatry The University of Melbourne and Melbourne Health Carlton South VIC Australia

Mental Health Research Center Moscow Russia

MR unit Department of Diagnostic and Interventional Radiology Institute for Clinical and Experimental Medicine Prague Czech Republic

National Institute of Mental Health Klecany Czech Republic

Neuroscience Institute Georgia State University Atlanta GA USA

Neuroscience Research Australia Sydney NSW Australia

Orygen Parkville VIC Australia

Priority Centre for Brain and Mental Health Research The University of Newcastle Newcastle NSW Australia

Priority Research Centre for Health Behaviour The University of Newcastle Newcastle NSW Australia

Psychiatric University Hospital Zurich Zurich Switzerland

Queensland Brain Institute The University of Queensland Brisbane QLD Australia

Research Institute of Clinical Medicine of Jeonbuk National University Biomedical Research Institute of Jeonbuk National University Hospital Jeonju Korea

School of Biomedical Sciences and Pharmacy University of Newcastle Newcastle NSW Australia

School of Medicine and Public Health The University of Newcastle Newcastle NSW Australia

School of Medicine University of Queensland Herston QLD Australia

School of Psychiatry University of New South Wales Sydney NSW Australia

School of Psychological Sciences University of Newcastle Callaghan NSW Australia

School of Psychology University of New South Wales Sydney NSW Australia

Stellenbosch University Genomics of Brain Disorders Research Unit South African Medical Research Council Cape Town South Africa

The Queensland Centre for Mental Health Research The University of Queensland Brisbane QLD Australia

Translational Developmental Neuroscience Section Division of Psychological and Social Medicine and Developmental Neurosciences Faculty of Medicine TU Dresden Germany

Tri institutional Center for Translational Research in Neuroimaging and Data Science Georgia State Georgia Tech Emory Atlanta GA USA

West Region Institute of Mental Health Singapore Singapore

Yong Loo Lin School of Medicine National University of Singapore Singapore Singapore

Zobrazit více v PubMed

Hjorthøj C, Stürup AE, McGrath JJ, Nordentoft M. Years of potential life lost and life expectancy in schizophrenia: a systematic review and meta-analysis. Lancet Psychiatry. 2017;4:295–301. PubMed

Olfson M, Gerhard T, Huang C, Crystal S, Stroup TS. Premature mortality among adults with schizophrenia in the United States. JAMA Psychiatry. 2015;72:1172–81. PubMed

Weye N, Momen NC, Christensen MK, Iburg KM, Dalsgaard S, Laursen TM, et al. Association of specific mental disorders with premature mortality in the danish population using alternative measurement methods. JAMA Netw Open. 2020;3:e206646. PubMed PMC

Correll CU, Solmi M, Veronese N, Bortolato B, Rosson S, Santonastaso P, et al. Prevalence, incidence and mortality from cardiovascular disease in patients with pooled and specific severe mental illness: a large-scale meta-analysis of 3,211,768 patients and 113,383,368 controls. World Psychiatry. 2017;16:163–80. PubMed PMC

Mitchell AJ, Vancampfort D, Sweers K, van Winkel R, Yu W, De Hert M. Prevalence of metabolic syndrome and metabolic abnormalities in schizophrenia and related disorders—a systematic review and meta-analysis. Schizophr Bull. 2013;39:306–18. PubMed PMC

Smith DJ, Langan J, McLean G, Guthrie B, Mercer SW. Schizophrenia is associated with excess multiple physical-health comorbidities but low levels of recorded cardiovascular disease in primary care: cross-sectional study. BMJ Open. 2013;3:e002808. PubMed PMC

Dieset I, Andreassen OA, Haukvik UK. Somatic comorbidity in schizophrenia: some possible biological mechanisms across the life span. Schizophr Bull. 2016;42:1316–9. PubMed PMC

Kirkpatrick B, Messias E, Harvey PD, Fernandez-Egea E, Bowie CR. Is schizophrenia a syndrome of accelerated aging? Schizophr Bull. 2008;34:1024–32. PubMed PMC

Stroup TS, Olfson M, Huang C, Wall MM, Goldberg T, Devanand DP, et al. Age-specific prevalence and incidence of dementia diagnoses among older US adults with schizophrenia. JAMA Psychiatry. 2021;78:632–41. PubMed PMC

Kirkpatrick B, Kennedy BK. Accelerated aging in schizophrenia and related disorders: future research. Schizophr Res. 2018;196:4–8. PubMed

Nguyen TT, Eyler LT, Jeste DV. Systemic biomarkers of accelerated aging in schizophrenia: a critical review and future directions. Schizophr Bull. 2018;44:398–408. PubMed PMC

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 NZ J Psychiatry. 2017;51:500–8. PubMed

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 PMC

Olabi B, Ellison-Wright I, McIntosh AM, Wood SJ, Bullmore E, Lawrie SM. Are there progressive brain changes in schizophrenia? a meta-analysis of structural magnetic resonance imaging studies. Biol Psychiatry. 2011;70:88–96. PubMed

Sun D, Stuart GW, Jenkinson M, Wood SJ, McGorry PD, Velakoulis D, et al. Brain surface contraction mapped in first-episode schizophrenia: a longitudinal magnetic resonance imaging study. Mol Psychiatry. 2008;14:976–86. PubMed PMC

Van Erp TGM, Hibar DP, Rasmussen JM, Glahn DC, Pearlson GD, Andreassen OA, et al. Subcortical brain volume abnormalities in 2028 individuals with schizophrenia and 2540 healthy controls via the ENIGMA consortium. Mol Psychiatry. 2016;21:547–53. PubMed PMC

van Erp TGM, Walton E, Hibar DP, Schmaal L, Jiang W, Glahn DC, et al. Cortical brain abnormalities in 4474 individuals with schizophrenia and 5098 control subjects via the Enhancing Neuro Imaging Genetics Through Meta Analysis (ENIGMA) Consortium. Biol Psychiatry. 2018;84:644–54. PubMed 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:e190. PubMed PMC

Cole JH, Franke K. Predicting age using neuroimaging: innovative brain ageing biomarkers. Trends Neurosci. 2017;40:681–90. PubMed

Beck D, de Lange AMG, Pedersen ML, Alnæs D, Maximov II, Voldsbekk I, et al. Cardiometabolic risk factors associated with brain age and accelerate brain ageing. Hum Brain Mapp. 10.1002/HBM.25680 2021. PubMed PMC

Cole JH. Multimodality neuroimaging brain-age in UK biobank: relationship to biomedical, lifestyle, and cognitive factors. Neurobiol Aging. 2020;92:34–42. PubMed PMC

Cole JH, Marioni RE, Harris SE, Deary IJ. Brain age and other bodily ‘ages’: implications for neuropsychiatry. Mol Psychiatry. 2019;24:266–81. PubMed PMC

Cole JH, Ritchie SJ, Bastin ME, Valdés Hernández MC, Muñoz Maniega S, Royle N, et al. Brain age predicts mortality. Mol Psychiatry. 2017;23:1385–92. PubMed PMC

Han LKM, Dinga R, Hahn T, Ching CRK, Eyler LT, Aftanas L, et al. Brain aging in major depressive disorder: results from the ENIGMA major depressive disorder working group. Mol Psychiatry. 2021;26:5124–39. PubMed PMC

Ning K, Zhao L, Matloff W, Sun F, Toga AW. Association of relative brain age with tobacco smoking, alcohol consumption, and genetic variants. Sci Rep. 2020;10:1–10. PubMed PMC

Hajek T, Franke K, Kolenic M, Capkova J, Matejka M, Propper L, et al. Brain age in early stages of bipolar disorders or schizophrenia. Schizophr Bull. 2019;45:191–8. PubMed PMC

Koutsouleris N, Davatzikos C, Borgwardt S, Gaser C, Bottlender R, Frodl T, et al. Accelerated brain aging in schizophrenia and beyond: a neuroanatomical marker of psychiatric disorders. Schizophr Bull. 2014;40:1140–53. PubMed PMC

Nenadić I, Dietzek M, Langbein K, Sauer H, Gaser C. BrainAGE score indicates accelerated brain aging in schizophrenia, but not bipolar disorder. Psychiatry Res—Neuroimaging. 2017;266:86–89. PubMed

Schnack HG, Van Haren NEM, Nieuwenhuis M, Pol HEH, Cahn W, Kahn RS. Accelerated brain aging in schizophrenia: a longitudinal pattern recognition study. Am J Psychiatry. 2016;173:607–16. PubMed

Shahab S, Mulsant BH, Levesque ML, Calarco N, Nazeri A, Wheeler AL, et al. Brain structure, cognition, and brain age in schizophrenia, bipolar disorder, and healthy controls. Neuropsychopharmacology. 2019;44:898–906. PubMed PMC

Wang J, Kochunov P, Sampath H, Hatch KS, Ryan MC, Xue F, et al. White matter brain aging in relationship to schizophrenia and its cognitive deficit. Schizophr Res. 2021;230:9–16. PubMed PMC

Kaufmann T, van der Meer D, Doan NT, Schwarz E, Lund MJ, Agartz I, et al. Common brain disorders are associated with heritable patterns of apparent aging of the brain. Nat Neurosci. 2019;22:1617–23. PubMed PMC

Tønnesen S, Kaufmann T, Lange A-MG, de, Richard G, Doan NT, Alnæs D, et al. Brain age prediction reveals aberrant brain white matter in schizophrenia and bipolar disorder: a multisample diffusion tensor imaging study. Biol Psychiatry Cogn Neurosci Neuroimaging. 2020;5:1095–103. PubMed

Fischl B. FreeSurfer. Neuroimage. 2012;62:774–81. PubMed PMC

Desikan RS, Ségonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, et al. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage. 2006;31:968–80. PubMed

Pedregosa F, Michel V, Grisel O, Blondel M, Prettenhofer P, Weiss R, et al. Scikit-learn: Machine Learning in Python. 12. 2011.

Le TT, Kuplicki RT, McKinney BA, Yeh H-W, Thompson WK, Paulus MP. A nonlinear simulation framework supports adjusting for age when analyzing BrainAGE. Front Aging Neurosci. 2018;10:317. PubMed PMC

Smith SM, Vidaurre D, Alfaro-Almagro F, Nichols TE, Miller KL. Estimation of brain age delta from brain imaging. Neuroimage. 2019;200:528–39. PubMed PMC

Viechtbauer W. Conducting meta-analyses in R with the metafor. J Stat Softw. 2010;36:1–48.

Baecker L, Dafflon J, da Costa PF, Garcia-Dias R, Vieira S, Scarpazza C, et al. Brain age prediction: a comparison between machine learning models using region- and voxel-based morphometric data. Hum Brain Mapp. 2021;42:2332–46. PubMed PMC

Lee WH, Antoniades M, Schnack HG, Kahn RS, Frangou S. Brain age prediction in schizophrenia: does the choice of machine learning algorithm matter? Psychiatry Res—Neuroimaging. 2021;310:111270. PubMed PMC

Ballester PL, Romano MT, de Azevedo Cardoso T, Hassel S, Strother SC, Kennedy SH, et al. Brain age in mood and psychotic disorders: a systematic review and meta-analysis. Acta Psychiatr Scand. 10.1111/ACPS.13371 2021. PubMed

Hibar DP, Westlye LT, Doan NT, Jahanshad N, Cheung JW, Ching CRK, et al. Cortical abnormalities in bipolar disorder: an MRI analysis of 6503 individuals from the ENIGMA Bipolar Disorder Working Group. Mol Psychiatry. 2018;23:932–42. PubMed PMC

Hibar DP, Westlye LT, Van Erp TGM, Rasmussen J, Leonardo CD, Faskowitz J, et al. Subcortical volumetric abnormalities in bipolar disorder. Mol Psychiatry. 2016;21:1710–6. PubMed PMC

Schmaal L, Veltman DJ, Van Erp TGM, Smann PG, Frodl T, Jahanshad N, et al. Subcortical brain alterations in major depressive disorder: findings from the ENIGMA Major Depressive Disorder working group. Mol Psychiatry. 2016;21:806–12. PubMed PMC

Schmaal L, Hibar DP, Sämann PG, Hall GB, Baune BT, Jahanshad N, et al. Cortical abnormalities in adults and adolescents with major depression based on brain scans from 20 cohorts worldwide in the ENIGMA Major Depressive Disorder Working Group. Mol Psychiatry. 2017;22:900–9. PubMed PMC

Vita A, De Peri L, Deste G, Barlati S, Sacchetti E. The effect of antipsychotic treatment on cortical gray matter changes in schizophrenia: does the class matter? A Meta-analysis and meta-regression of longitudinal magnetic resonance imaging studies. Biol Psychiatry. 2015;78:403–12. PubMed

Smieskova R, Fusar-Poli P, Allen P, Bendfeldt K, Stieglitz R, Drewe J, et al. The effects of antipsychotics on the brain: what have we learnt from structural imaging of schizophrenia?—A systematic review. Curr Pharm Des. 2009;15:2535–49. PubMed

McWhinney S, Kolenic M, Franke K, Fialova M, Knytl P, Matejka M, et al. Obesity as a risk factor for accelerated brain ageing in first-episode psychosis—a longitudinal study. Schizophr Bull. 2021;47:1772–81. PubMed PMC

Mattson MP, Arumugam TV. Hallmarks of brain aging: adaptive and pathological modification by metabolic states. Cell Metab. 2018;27:1176–99. PubMed PMC

Kirkpatrick B, Miller BJ. Inflammation and schizophrenia. Schizophr Bull. 2013;39:1174–9. PubMed PMC

Miller BJ, Goldsmith DR. Inflammatory biomarkers in schizophrenia: Implications for heterogeneity and neurobiology. Biomark Neuropsychiatry. 2019;1:100006.

Wu D, Lv P, Li F, Zhang W, Fu G, Dai J, et al. Association of peripheral cytokine levels with cerebral structural abnormalities in schizophrenia. Brain Res. 2019;1724:146463. PubMed

Franke K, Gaser C, Manor B, Novak V. Advanced BrainAGE in older adults with type 2 diabetes mellitus. Front Aging Neurosci. 2013;5:90. PubMed PMC

Yao JK, Leonard S, Reddy RD. Increased nitric oxide radicals in postmortem brain from patients with schizophrenia. Schizophr Bull. 2004;30:923–34. PubMed

Okusaga OO. Accelerated aging in schizophrenia patients: the potential role of oxidative stress. Aging Dis. 2014;5:256–62. PubMed PMC

Butler ER, Chen A, Ramadan R, Le TT, Ruparel K, Moore TM, et al. Pitfalls in brain age analyses. Hum Brain Mapp. 2021;42:4092–101. PubMed PMC

de Lange AMG, Anatürk M, Rokicki J, Han LKM, Franke K, Alnæs D, et al. Mind the gap: performance metric evaluation in brain-age prediction. Hum Brain Mapp. 2022;43:3113–29. PubMed PMC

van der Velden BHM, Kuijf HJ, Gilhuijs KGA, Viergever MA. Explainable artificial intelligence (XAI) in deep learning-based medical image analysis. Med Image Anal. 2022;79:102470. PubMed

Popescu SG, Glocker B, Sharp DJ, Cole JH. Local Brain-Age: A U-Net model. Front Aging Neurosci. 2021;13:838. PubMed PMC

Vidal-Pineiro D, Wang Y, Krogsrud SK, Amlien IK, Baaré WFC, Bartres-Faz D, et al. Individual variations in ‘brain age’ relate to early-life factors more than to longitudinal brain change. Elife. 2021;10:e69995. PubMed PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...