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Meta-Analysis
. 2018 Nov 1;84(9):644-654.
doi: 10.1016/j.biopsych.2018.04.023. Epub 2018 May 14.

Cortical Brain Abnormalities in 4474 Individuals With Schizophrenia and 5098 Control Subjects via the Enhancing Neuro Imaging Genetics Through Meta Analysis (ENIGMA) Consortium

Theo G M van Erp  1 Esther Walton  2 Derrek P Hibar  3 Lianne Schmaal  4 Wenhao Jiang  5 David C Glahn  6 Godfrey D Pearlson  6 Nailin Yao  6 Masaki Fukunaga  7 Ryota Hashimoto  8 Naohiro Okada  9 Hidenaga Yamamori  10 Juan R Bustillo  11 Vincent P Clark  12 Ingrid Agartz  13 Bryon A Mueller  14 Wiepke Cahn  15 Sonja M C de Zwarte  15 Hilleke E Hulshoff Pol  15 René S Kahn  15 Roel A Ophoff  16 Neeltje E M van Haren  17 Ole A Andreassen  18 Anders M Dale  19 Nhat Trung Doan  20 Tiril P Gurholt  21 Cecilie B Hartberg  20 Unn K Haukvik  18 Kjetil N Jørgensen  21 Trine V Lagerberg  22 Ingrid Melle  18 Lars T Westlye  23 Oliver Gruber  24 Bernd Kraemer  24 Anja Richter  24 David Zilles  25 Vince D Calhoun  12 Benedicto Crespo-Facorro  26 Roberto Roiz-Santiañez  26 Diana Tordesillas-Gutiérrez  27 Carmel Loughland  28 Vaughan J Carr  29 Stanley Catts  30 Vanessa L Cropley  31 Janice M Fullerton  32 Melissa J Green  33 Frans A Henskens  34 Assen Jablensky  35 Rhoshel K Lenroot  33 Bryan J Mowry  36 Patricia T Michie  37 Christos Pantelis  38 Yann Quidé  33 Ulrich Schall  39 Rodney J Scott  40 Murray J Cairns  40 Marc Seal  41 Paul A Tooney  42 Paul E Rasser  43 Gavin Cooper  43 Cynthia Shannon Weickert  33 Thomas W Weickert  33 Derek W Morris  44 Elliot Hong  45 Peter Kochunov  45 Lauren M Beard  46 Raquel E Gur  46 Ruben C Gur  46 Theodore D Satterthwaite  46 Daniel H Wolf  46 Aysenil Belger  47 Gregory G Brown  48 Judith M Ford  49 Fabio Macciardi  50 Daniel H Mathalon  49 Daniel S O'Leary  51 Steven G Potkin  50 Adrian Preda  50 James Voyvodic  52 Kelvin O Lim  14 Sarah McEwen  53 Fude Yang  54 Yunlong Tan  54 Shuping Tan  54 Zhiren Wang  54 Fengmei Fan  54 Jingxu Chen  54 Hong Xiang  55 Shiyou Tang  55 Hua Guo  56 Ping Wan  56 Dong Wei  57 Henry J Bockholt  58 Stefan Ehrlich  59 Rick P F Wolthusen  60 Margaret D King  61 Jody M Shoemaker  61 Scott R Sponheim  62 Lieuwe De Haan  63 Laura Koenders  63 Marise W Machielsen  63 Therese van Amelsvoort  64 Dick J Veltman  65 Francesca Assogna  66 Nerisa Banaj  67 Pietro de Rossi  68 Mariangela Iorio  67 Fabrizio Piras  66 Gianfranco Spalletta  69 Peter J McKenna  70 Edith Pomarol-Clotet  70 Raymond Salvador  70 Aiden Corvin  71 Gary Donohoe  44 Sinead Kelly  72 Christopher D Whelan  73 Erin W Dickie  74 David Rotenberg  74 Aristotle N Voineskos  74 Simone Ciufolini  75 Joaquim Radua  76 Paola Dazzan  77 Robin Murray  75 Tiago Reis Marques  75 Andrew Simmons  75 Stefan Borgwardt  78 Laura Egloff  78 Fabienne Harrisberger  78 Anita Riecher-Rössler  78 Renata Smieskova  78 Kathryn I Alpert  79 Lei Wang  80 Erik G Jönsson  81 Sanne Koops  15 Iris E C Sommer  82 Alessandro Bertolino  83 Aurora Bonvino  84 Annabella Di Giorgio  84 Emma Neilson  85 Andrew R Mayer  61 Julia M Stephen  61 Jun Soo Kwon  86 Je-Yeon Yun  87 Dara M Cannon  88 Colm McDonald  88 Irina Lebedeva  89 Alexander S Tomyshev  89 Tolibjohn Akhadov  90 Vasily Kaleda  89 Helena Fatouros-Bergman  91 Lena Flyckt  91 Karolinska Schizophrenia ProjectGeraldo F Busatto  92 Pedro G P Rosa  92 Mauricio H Serpa  92 Marcus V Zanetti  92 Cyril Hoschl  93 Antonin Skoch  94 Filip Spaniel  93 David Tomecek  95 Saskia P Hagenaars  96 Andrew M McIntosh  97 Heather C Whalley  85 Stephen M Lawrie  85 Christian Knöchel  98 Viola Oertel-Knöchel  98 Michael Stäblein  98 Fleur M Howells  99 Dan J Stein  100 Henk S Temmingh  99 Anne Uhlmann  101 Carlos Lopez-Jaramillo  102 Danai Dima  103 Agnes McMahon  73 Joshua I Faskowitz  73 Boris A Gutman  104 Neda Jahanshad  73 Paul M Thompson  73 Jessica A Turner  105
Collaborators, Affiliations
Free PMC article
Meta-Analysis

Cortical Brain Abnormalities in 4474 Individuals With Schizophrenia and 5098 Control Subjects via the Enhancing Neuro Imaging Genetics Through Meta Analysis (ENIGMA) Consortium

Theo G M van Erp et al. Biol Psychiatry. .
Free PMC article

Abstract

Background: The profile of cortical neuroanatomical abnormalities in schizophrenia is not fully understood, despite hundreds of published structural brain imaging studies. This study presents the first meta-analysis of cortical thickness and surface area abnormalities in schizophrenia conducted by the ENIGMA (Enhancing Neuro Imaging Genetics through Meta Analysis) Schizophrenia Working Group.

Methods: The study included data from 4474 individuals with schizophrenia (mean age, 32.3 years; range, 11-78 years; 66% male) and 5098 healthy volunteers (mean age, 32.8 years; range, 10-87 years; 53% male) assessed with standardized methods at 39 centers worldwide.

Results: Compared with healthy volunteers, individuals with schizophrenia have widespread thinner cortex (left/right hemisphere: Cohen's d = -0.530/-0.516) and smaller surface area (left/right hemisphere: Cohen's d = -0.251/-0.254), with the largest effect sizes for both in frontal and temporal lobe regions. Regional group differences in cortical thickness remained significant when statistically controlling for global cortical thickness, suggesting regional specificity. In contrast, effects for cortical surface area appear global. Case-control, negative, cortical thickness effect sizes were two to three times larger in individuals receiving antipsychotic medication relative to unmedicated individuals. Negative correlations between age and bilateral temporal pole thickness were stronger in individuals with schizophrenia than in healthy volunteers. Regional cortical thickness showed significant negative correlations with normalized medication dose, symptom severity, and duration of illness and positive correlations with age at onset.

Conclusions: The findings indicate that the ENIGMA meta-analysis approach can achieve robust findings in clinical neuroscience studies; also, medication effects should be taken into account in future genetic association studies of cortical thickness in schizophrenia.

Keywords: Cortical; Imaging; Meta-analysis; Schizophrenia; Surface area; Thickness.

Conflict of interest statement

CONFLICTS OF INTEREST

Dr. Van Erp has had a research contract with Otsuka Pharmaceuticals, Inc. Adrian Preda has served as a consultant for Boehringer Ingelheim. The remaining authors report no biomedical financial interests or potential conflicts of interest.

Figures

Figure 1.
Figure 1.
Cortical map of regional Cohen’s d effect sizes for schizophrenia versus healthy group cortical thickness contrast statistically controlling for A) age and sex, and B) age, sex, and global cortical thickness. Only regions with pFDR<0.05 are depicted in color. In figure 1B, warm colors (yellow-red) reflect regions in which the effect of schizophrenia is more than than the mean global cortical thinning, and cool colors (green-blue) reflect regions where the effect of schizophrenia is less than the mean global thinning compared to controls.
Figure 2.
Figure 2.
Cohen’s d effect sizes for schizophrenia versus healthy group cortical thickness contrast statistically controlling for age, sex, and global mean cortical thickness. Only regions with pFDR<0.05 are depicted in color.
Figure 3.
Figure 3.
Cortical map of regional Cohen’s d effect sizes for schizophrenia versus healthy group cortical surface area contrast statistically controlling for A) age and sex, and B) age, sex, and total cortical surface area. Only regions with pFDR<0.05 are depicted in color. In figure 3B, warm colors (yellow-red) would reflect regions in which the effect of schizophrenia is more than the mean lower lower surface area, and cool colors (green-blue) reflect regions where the effect of schizophrenia is less than the mean lower global surface area compared to controls.
Figure 4.
Figure 4.
A) Cohen’s d effect sizes, and B) least square mean percent difference for schizophrenia versus healthy group contrasts in global cortical thickness, statistically controlling for age, and sex, by medication group and hemisphere. Nominal one-tailed p-values for left (L) and right (R) hemisphere thickness group comparisons, statistically controlling for age and sex, were: Second-Generation vs. Unmedicated [p(L)<0.05; p(R)<0.06]; First-Generation vs. Unmedicated [p(L)<0.01; p(R)<0.002]; Both First-Generation and Second-Generation vs. Unmedicated [p(L)<0.02; p<0.05]; First-Generation vs. Second-Generation [p(L)<0.03; p(R)<0.03]; Both First-Generation and Second-Generation vs. Second-Generation [p(L)<0.02; p(R)<0.05]; Both First-Generation and Second-Generation vs. First-Generation [p(L)=0.50; p(R)=0.48]; Supplementary Tables S16–S21).

Comment in

  • The Power of Collaboration and Data Aggregation.
    Barch DM. Barch DM. Biol Psychiatry. 2018 Nov 1;84(9):626-628. doi: 10.1016/j.biopsych.2018.06.005. Biol Psychiatry. 2018. PMID: 30297020 No abstract available.
  • New Meta- and Mega-analyses of Magnetic Resonance Imaging Findings in Schizophrenia: Do They Really Increase Our Knowledge About the Nature of the Disease Process?
    Vita A, De Peri L. Vita A, et al. Biol Psychiatry. 2019 Apr 1;85(7):e33. doi: 10.1016/j.biopsych.2018.07.029. Epub 2018 Nov 22. Biol Psychiatry. 2019. PMID: 30470560 No abstract available.
  • Reply to: New Meta- and Mega-analyses of Magnetic Resonance Imaging Findings in Schizophrenia: Do They Really Increase Our Knowledge About the Nature of the Disease Process?
    van Erp TGM, Walton E, Hibar DP, Schmaal L, Jiang W, Glahn DC, Pearlson GD, Yao N, Fukunaga M, Hashimoto R, Okada N, Yamamori H, Clark VP, Mueller BA, de Zwarte SMC, Ophoff RA, van Haren NEM, Andreassen OA, Gurholt TP, Gruber O, Kraemer B, Richter A, Calhoun VD, Crespo-Facorro B, Roiz-Santiañez R, Tordesillas-Gutiérrez D, Loughland C, Catts S, Fullerton JM, Green MJ, Henskens F, Jablensky A, Mowry BJ, Pantelis C, Quidé Y, Schall U, Scott RJ, Cairns MJ, Seal M, Tooney PA, Rasser PE, Cooper G, Shannon Weickert C, Weickert TW, Hong E, Kochunov P, Gur RE, Gur RC, Ford JM, Macciardi F, Mathalon DH, Potkin SG, Preda A, Fan F, Ehrlich S, King MD, De Haan L, Veltman DJ, Assogna F, Banaj N, de Rossi P, Iorio M, Piras F, Spalletta G, Pomarol-Clotet E, Kelly S, Ciufolini S, Radua J, Murray R, Marques TR, Simmons A, Borgwardt S, Schönborn-Harrisberger F, Riecher-Rössler A, Smieskova R, Alpert KI, Bertolino A, Bonvino A, Di Giorgio A, Neilson E, Mayer AR, Yun JY, Cannon DM, Lebedeva I, Tomyshev AS, Akhadov T, Kaleda V, Fatouros-Bergman H, Flyckt L; Karolinska Schizophrenia Project, Rosa PGP, Serpa MH, Zanetti MV, Hoschl C, Skoch A, Spaniel F, Tomecek D, McIntosh AM, Whalley HC, Knöchel C, Oertel-Knöchel V, Howells FM, Stein DJ, Temmingh HS, Uhlmann A, Lopez-Jaramillo C, Dima D, Faskowitz JI, Gutman BA, Jahanshad N, Thompson PM, Turner JA. van Erp TGM, et al. Biol Psychiatry. 2019 Apr 1;85(7):e35-e39. doi: 10.1016/j.biopsych.2018.10.003. Epub 2018 Nov 22. Biol Psychiatry. 2019. PMID: 30470561 Free PMC article. No abstract available.

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