The Association Between Familial Risk and Brain Abnormalities Is Disease Specific: An ENIGMA-Relatives Study of Schizophrenia and Bipolar Disorder

Sonja M.C. de Zwarte, Rachel M. Brouwer, Ingrid Agartz, Martin Alda, André Aleman, Kathryn I. Alpert, Carrie E. Bearden, Alessandro Bertolino, Catherine Bois, Aurora Bonvino, Elvira Bramon, Elizabeth E.L. Buimer, Wiepke Cahn, Dara M. Cannon, Tyrone D. Cannon, Xavier Caseras, Josefina Castro-Fornieles, Qiang Chen, Yoonho Chung, Elena De la SernaAnnabella Di Giorgio, Gaelle E. Doucet, Mehmet Cagdas Eker, Susanne Erk, Scott C. Fears, Sonya F. Foley, Sophia Frangou, Andrew Frankland, Janice M. Fullerton, David C. Glahn, Vina M. Goghari, Aaron L. Goldman, Ali Saffet Gonul, Oliver Gruber, Lieuwe de Haan, Tomas Hajek, Emma L. Hawkins, Andreas Heinz, Manon H.J. Hillegers, Hilleke E. Hulshoff Pol, Christina M. Hultman, Martin Ingvar, Viktoria Johansson, Erik G. Jönsson, Fergus Kane, Matthew J. Kempton, Marinka M.G. Koenis, Miloslav Kopecek, Lydia Krabbendam, Bernd Krämer, Stephen M. Lawrie, Rhoshel K. Lenroot, Machteld Marcelis, Jan Bernard C. Marsman, Venkata S. Mattay, Colm McDonald, Andreas Meyer-Lindenberg, Stijn Michielse, Philip B. Mitchell, Dolores Moreno, Robin M. Murray, Benson Mwangi, Pablo Najt, Emma Neilson, Jason Newport, Jim van Os, Bronwyn Overs, Aysegul Ozerdem, Marco M. Picchioni, Anja Richter, Gloria Roberts, Aybala Saricicek Aydogan, Peter R. Schofield, Fatma Simsek, Jair C. Soares, Gisela Sugranyes, Timothea Toulopoulou, Giulia Tronchin, Henrik Walter, Lei Wang, Daniel R. Weinberger, Heather C. Whalley, Nefize Yalin, Ole A. Andreassen, Christopher R.K. Ching, Theo G.M. van Erp, Jessica A. Turner, Neda Jahanshad, Paul M. Thompson, René S. Kahn, Neeltje E.M. van Haren

Research output: Contribution to journalArticle

Abstract

Background: Schizophrenia and bipolar disorder share genetic liability, and some structural brain abnormalities are common to both conditions. First-degree relatives of patients with schizophrenia (FDRs-SZ) show similar brain abnormalities to patients, albeit with smaller effect sizes. Imaging findings in first-degree relatives of patients with bipolar disorder (FDRs-BD) have been inconsistent in the past, but recent studies report regionally greater volumes compared with control subjects. Methods: We performed a meta-analysis of global and subcortical brain measures of 6008 individuals (1228 FDRs-SZ, 852 FDRs-BD, 2246 control subjects, 1016 patients with schizophrenia, 666 patients with bipolar disorder) from 34 schizophrenia and/or bipolar disorder family cohorts with standardized methods. Analyses were repeated with a correction for intracranial volume (ICV) and for the presence of any psychopathology in the relatives and control subjects. Results: FDRs-BD had significantly larger ICV (d = +0.16, q <.05 corrected), whereas FDRs-SZ showed smaller thalamic volumes than control subjects (d = −0.12, q <.05 corrected). ICV explained the enlargements in the brain measures in FDRs-BD. In FDRs-SZ, after correction for ICV, total brain, cortical gray matter, cerebral white matter, cerebellar gray and white matter, and thalamus volumes were significantly smaller; the cortex was thinner (d < −0.09, q <.05 corrected); and third ventricle was larger (d = +0.15, q <.05 corrected). The findings were not explained by psychopathology in the relatives or control subjects. Conclusions: Despite shared genetic liability, FDRs-SZ and FDRs-BD show a differential pattern of structural brain abnormalities, specifically a divergent effect in ICV. This may imply that the neurodevelopmental trajectories leading to brain anomalies in schizophrenia or bipolar disorder are distinct.

Original languageEnglish (US)
Pages (from-to)545-556
Number of pages12
JournalBiological psychiatry
Volume86
Issue number7
DOIs
StatePublished - Oct 1 2019

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Bipolar Disorder
Schizophrenia
Brain
Psychopathology
Third Ventricle
Thalamus
Meta-Analysis

Keywords

  • Bipolar disorder
  • Familial risk
  • Imaging
  • Meta-analysis
  • Neurodevelopment
  • Schizophrenia

ASJC Scopus subject areas

  • Biological Psychiatry

Cite this

The Association Between Familial Risk and Brain Abnormalities Is Disease Specific : An ENIGMA-Relatives Study of Schizophrenia and Bipolar Disorder. / de Zwarte, Sonja M.C.; Brouwer, Rachel M.; Agartz, Ingrid; Alda, Martin; Aleman, André; Alpert, Kathryn I.; Bearden, Carrie E.; Bertolino, Alessandro; Bois, Catherine; Bonvino, Aurora; Bramon, Elvira; Buimer, Elizabeth E.L.; Cahn, Wiepke; Cannon, Dara M.; Cannon, Tyrone D.; Caseras, Xavier; Castro-Fornieles, Josefina; Chen, Qiang; Chung, Yoonho; De la Serna, Elena; Di Giorgio, Annabella; Doucet, Gaelle E.; Eker, Mehmet Cagdas; Erk, Susanne; Fears, Scott C.; Foley, Sonya F.; Frangou, Sophia; Frankland, Andrew; Fullerton, Janice M.; Glahn, David C.; Goghari, Vina M.; Goldman, Aaron L.; Gonul, Ali Saffet; Gruber, Oliver; de Haan, Lieuwe; Hajek, Tomas; Hawkins, Emma L.; Heinz, Andreas; Hillegers, Manon H.J.; Hulshoff Pol, Hilleke E.; Hultman, Christina M.; Ingvar, Martin; Johansson, Viktoria; Jönsson, Erik G.; Kane, Fergus; Kempton, Matthew J.; Koenis, Marinka M.G.; Kopecek, Miloslav; Krabbendam, Lydia; Krämer, Bernd; Lawrie, Stephen M.; Lenroot, Rhoshel K.; Marcelis, Machteld; Marsman, Jan Bernard C.; Mattay, Venkata S.; McDonald, Colm; Meyer-Lindenberg, Andreas; Michielse, Stijn; Mitchell, Philip B.; Moreno, Dolores; Murray, Robin M.; Mwangi, Benson; Najt, Pablo; Neilson, Emma; Newport, Jason; van Os, Jim; Overs, Bronwyn; Ozerdem, Aysegul; Picchioni, Marco M.; Richter, Anja; Roberts, Gloria; Aydogan, Aybala Saricicek; Schofield, Peter R.; Simsek, Fatma; Soares, Jair C.; Sugranyes, Gisela; Toulopoulou, Timothea; Tronchin, Giulia; Walter, Henrik; Wang, Lei; Weinberger, Daniel R.; Whalley, Heather C.; Yalin, Nefize; Andreassen, Ole A.; Ching, Christopher R.K.; van Erp, Theo G.M.; Turner, Jessica A.; Jahanshad, Neda; Thompson, Paul M.; Kahn, René S.; van Haren, Neeltje E.M.

In: Biological psychiatry, Vol. 86, No. 7, 01.10.2019, p. 545-556.

Research output: Contribution to journalArticle

de Zwarte, SMC, Brouwer, RM, Agartz, I, Alda, M, Aleman, A, Alpert, KI, Bearden, CE, Bertolino, A, Bois, C, Bonvino, A, Bramon, E, Buimer, EEL, Cahn, W, Cannon, DM, Cannon, TD, Caseras, X, Castro-Fornieles, J, Chen, Q, Chung, Y, De la Serna, E, Di Giorgio, A, Doucet, GE, Eker, MC, Erk, S, Fears, SC, Foley, SF, Frangou, S, Frankland, A, Fullerton, JM, Glahn, DC, Goghari, VM, Goldman, AL, Gonul, AS, Gruber, O, de Haan, L, Hajek, T, Hawkins, EL, Heinz, A, Hillegers, MHJ, Hulshoff Pol, HE, Hultman, CM, Ingvar, M, Johansson, V, Jönsson, EG, Kane, F, Kempton, MJ, Koenis, MMG, Kopecek, M, Krabbendam, L, Krämer, B, Lawrie, SM, Lenroot, RK, Marcelis, M, Marsman, JBC, Mattay, VS, McDonald, C, Meyer-Lindenberg, A, Michielse, S, Mitchell, PB, Moreno, D, Murray, RM, Mwangi, B, Najt, P, Neilson, E, Newport, J, van Os, J, Overs, B, Ozerdem, A, Picchioni, MM, Richter, A, Roberts, G, Aydogan, AS, Schofield, PR, Simsek, F, Soares, JC, Sugranyes, G, Toulopoulou, T, Tronchin, G, Walter, H, Wang, L, Weinberger, DR, Whalley, HC, Yalin, N, Andreassen, OA, Ching, CRK, van Erp, TGM, Turner, JA, Jahanshad, N, Thompson, PM, Kahn, RS & van Haren, NEM 2019, 'The Association Between Familial Risk and Brain Abnormalities Is Disease Specific: An ENIGMA-Relatives Study of Schizophrenia and Bipolar Disorder', Biological psychiatry, vol. 86, no. 7, pp. 545-556. https://doi.org/10.1016/j.biopsych.2019.03.985
de Zwarte, Sonja M.C. ; Brouwer, Rachel M. ; Agartz, Ingrid ; Alda, Martin ; Aleman, André ; Alpert, Kathryn I. ; Bearden, Carrie E. ; Bertolino, Alessandro ; Bois, Catherine ; Bonvino, Aurora ; Bramon, Elvira ; Buimer, Elizabeth E.L. ; Cahn, Wiepke ; Cannon, Dara M. ; Cannon, Tyrone D. ; Caseras, Xavier ; Castro-Fornieles, Josefina ; Chen, Qiang ; Chung, Yoonho ; De la Serna, Elena ; Di Giorgio, Annabella ; Doucet, Gaelle E. ; Eker, Mehmet Cagdas ; Erk, Susanne ; Fears, Scott C. ; Foley, Sonya F. ; Frangou, Sophia ; Frankland, Andrew ; Fullerton, Janice M. ; Glahn, David C. ; Goghari, Vina M. ; Goldman, Aaron L. ; Gonul, Ali Saffet ; Gruber, Oliver ; de Haan, Lieuwe ; Hajek, Tomas ; Hawkins, Emma L. ; Heinz, Andreas ; Hillegers, Manon H.J. ; Hulshoff Pol, Hilleke E. ; Hultman, Christina M. ; Ingvar, Martin ; Johansson, Viktoria ; Jönsson, Erik G. ; Kane, Fergus ; Kempton, Matthew J. ; Koenis, Marinka M.G. ; Kopecek, Miloslav ; Krabbendam, Lydia ; Krämer, Bernd ; Lawrie, Stephen M. ; Lenroot, Rhoshel K. ; Marcelis, Machteld ; Marsman, Jan Bernard C. ; Mattay, Venkata S. ; McDonald, Colm ; Meyer-Lindenberg, Andreas ; Michielse, Stijn ; Mitchell, Philip B. ; Moreno, Dolores ; Murray, Robin M. ; Mwangi, Benson ; Najt, Pablo ; Neilson, Emma ; Newport, Jason ; van Os, Jim ; Overs, Bronwyn ; Ozerdem, Aysegul ; Picchioni, Marco M. ; Richter, Anja ; Roberts, Gloria ; Aydogan, Aybala Saricicek ; Schofield, Peter R. ; Simsek, Fatma ; Soares, Jair C. ; Sugranyes, Gisela ; Toulopoulou, Timothea ; Tronchin, Giulia ; Walter, Henrik ; Wang, Lei ; Weinberger, Daniel R. ; Whalley, Heather C. ; Yalin, Nefize ; Andreassen, Ole A. ; Ching, Christopher R.K. ; van Erp, Theo G.M. ; Turner, Jessica A. ; Jahanshad, Neda ; Thompson, Paul M. ; Kahn, René S. ; van Haren, Neeltje E.M. / The Association Between Familial Risk and Brain Abnormalities Is Disease Specific : An ENIGMA-Relatives Study of Schizophrenia and Bipolar Disorder. In: Biological psychiatry. 2019 ; Vol. 86, No. 7. pp. 545-556.
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abstract = "Background: Schizophrenia and bipolar disorder share genetic liability, and some structural brain abnormalities are common to both conditions. First-degree relatives of patients with schizophrenia (FDRs-SZ) show similar brain abnormalities to patients, albeit with smaller effect sizes. Imaging findings in first-degree relatives of patients with bipolar disorder (FDRs-BD) have been inconsistent in the past, but recent studies report regionally greater volumes compared with control subjects. Methods: We performed a meta-analysis of global and subcortical brain measures of 6008 individuals (1228 FDRs-SZ, 852 FDRs-BD, 2246 control subjects, 1016 patients with schizophrenia, 666 patients with bipolar disorder) from 34 schizophrenia and/or bipolar disorder family cohorts with standardized methods. Analyses were repeated with a correction for intracranial volume (ICV) and for the presence of any psychopathology in the relatives and control subjects. Results: FDRs-BD had significantly larger ICV (d = +0.16, q <.05 corrected), whereas FDRs-SZ showed smaller thalamic volumes than control subjects (d = −0.12, q <.05 corrected). ICV explained the enlargements in the brain measures in FDRs-BD. In FDRs-SZ, after correction for ICV, total brain, cortical gray matter, cerebral white matter, cerebellar gray and white matter, and thalamus volumes were significantly smaller; the cortex was thinner (d < −0.09, q <.05 corrected); and third ventricle was larger (d = +0.15, q <.05 corrected). The findings were not explained by psychopathology in the relatives or control subjects. Conclusions: Despite shared genetic liability, FDRs-SZ and FDRs-BD show a differential pattern of structural brain abnormalities, specifically a divergent effect in ICV. This may imply that the neurodevelopmental trajectories leading to brain anomalies in schizophrenia or bipolar disorder are distinct.",
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TY - JOUR

T1 - The Association Between Familial Risk and Brain Abnormalities Is Disease Specific

T2 - An ENIGMA-Relatives Study of Schizophrenia and Bipolar Disorder

AU - de Zwarte, Sonja M.C.

AU - Brouwer, Rachel M.

AU - Agartz, Ingrid

AU - Alda, Martin

AU - Aleman, André

AU - Alpert, Kathryn I.

AU - Bearden, Carrie E.

AU - Bertolino, Alessandro

AU - Bois, Catherine

AU - Bonvino, Aurora

AU - Bramon, Elvira

AU - Buimer, Elizabeth E.L.

AU - Cahn, Wiepke

AU - Cannon, Dara M.

AU - Cannon, Tyrone D.

AU - Caseras, Xavier

AU - Castro-Fornieles, Josefina

AU - Chen, Qiang

AU - Chung, Yoonho

AU - De la Serna, Elena

AU - Di Giorgio, Annabella

AU - Doucet, Gaelle E.

AU - Eker, Mehmet Cagdas

AU - Erk, Susanne

AU - Fears, Scott C.

AU - Foley, Sonya F.

AU - Frangou, Sophia

AU - Frankland, Andrew

AU - Fullerton, Janice M.

AU - Glahn, David C.

AU - Goghari, Vina M.

AU - Goldman, Aaron L.

AU - Gonul, Ali Saffet

AU - Gruber, Oliver

AU - de Haan, Lieuwe

AU - Hajek, Tomas

AU - Hawkins, Emma L.

AU - Heinz, Andreas

AU - Hillegers, Manon H.J.

AU - Hulshoff Pol, Hilleke E.

AU - Hultman, Christina M.

AU - Ingvar, Martin

AU - Johansson, Viktoria

AU - Jönsson, Erik G.

AU - Kane, Fergus

AU - Kempton, Matthew J.

AU - Koenis, Marinka M.G.

AU - Kopecek, Miloslav

AU - Krabbendam, Lydia

AU - Krämer, Bernd

AU - Lawrie, Stephen M.

AU - Lenroot, Rhoshel K.

AU - Marcelis, Machteld

AU - Marsman, Jan Bernard C.

AU - Mattay, Venkata S.

AU - McDonald, Colm

AU - Meyer-Lindenberg, Andreas

AU - Michielse, Stijn

AU - Mitchell, Philip B.

AU - Moreno, Dolores

AU - Murray, Robin M.

AU - Mwangi, Benson

AU - Najt, Pablo

AU - Neilson, Emma

AU - Newport, Jason

AU - van Os, Jim

AU - Overs, Bronwyn

AU - Ozerdem, Aysegul

AU - Picchioni, Marco M.

AU - Richter, Anja

AU - Roberts, Gloria

AU - Aydogan, Aybala Saricicek

AU - Schofield, Peter R.

AU - Simsek, Fatma

AU - Soares, Jair C.

AU - Sugranyes, Gisela

AU - Toulopoulou, Timothea

AU - Tronchin, Giulia

AU - Walter, Henrik

AU - Wang, Lei

AU - Weinberger, Daniel R.

AU - Whalley, Heather C.

AU - Yalin, Nefize

AU - Andreassen, Ole A.

AU - Ching, Christopher R.K.

AU - van Erp, Theo G.M.

AU - Turner, Jessica A.

AU - Jahanshad, Neda

AU - Thompson, Paul M.

AU - Kahn, René S.

AU - van Haren, Neeltje E.M.

PY - 2019/10/1

Y1 - 2019/10/1

N2 - Background: Schizophrenia and bipolar disorder share genetic liability, and some structural brain abnormalities are common to both conditions. First-degree relatives of patients with schizophrenia (FDRs-SZ) show similar brain abnormalities to patients, albeit with smaller effect sizes. Imaging findings in first-degree relatives of patients with bipolar disorder (FDRs-BD) have been inconsistent in the past, but recent studies report regionally greater volumes compared with control subjects. Methods: We performed a meta-analysis of global and subcortical brain measures of 6008 individuals (1228 FDRs-SZ, 852 FDRs-BD, 2246 control subjects, 1016 patients with schizophrenia, 666 patients with bipolar disorder) from 34 schizophrenia and/or bipolar disorder family cohorts with standardized methods. Analyses were repeated with a correction for intracranial volume (ICV) and for the presence of any psychopathology in the relatives and control subjects. Results: FDRs-BD had significantly larger ICV (d = +0.16, q <.05 corrected), whereas FDRs-SZ showed smaller thalamic volumes than control subjects (d = −0.12, q <.05 corrected). ICV explained the enlargements in the brain measures in FDRs-BD. In FDRs-SZ, after correction for ICV, total brain, cortical gray matter, cerebral white matter, cerebellar gray and white matter, and thalamus volumes were significantly smaller; the cortex was thinner (d < −0.09, q <.05 corrected); and third ventricle was larger (d = +0.15, q <.05 corrected). The findings were not explained by psychopathology in the relatives or control subjects. Conclusions: Despite shared genetic liability, FDRs-SZ and FDRs-BD show a differential pattern of structural brain abnormalities, specifically a divergent effect in ICV. This may imply that the neurodevelopmental trajectories leading to brain anomalies in schizophrenia or bipolar disorder are distinct.

AB - Background: Schizophrenia and bipolar disorder share genetic liability, and some structural brain abnormalities are common to both conditions. First-degree relatives of patients with schizophrenia (FDRs-SZ) show similar brain abnormalities to patients, albeit with smaller effect sizes. Imaging findings in first-degree relatives of patients with bipolar disorder (FDRs-BD) have been inconsistent in the past, but recent studies report regionally greater volumes compared with control subjects. Methods: We performed a meta-analysis of global and subcortical brain measures of 6008 individuals (1228 FDRs-SZ, 852 FDRs-BD, 2246 control subjects, 1016 patients with schizophrenia, 666 patients with bipolar disorder) from 34 schizophrenia and/or bipolar disorder family cohorts with standardized methods. Analyses were repeated with a correction for intracranial volume (ICV) and for the presence of any psychopathology in the relatives and control subjects. Results: FDRs-BD had significantly larger ICV (d = +0.16, q <.05 corrected), whereas FDRs-SZ showed smaller thalamic volumes than control subjects (d = −0.12, q <.05 corrected). ICV explained the enlargements in the brain measures in FDRs-BD. In FDRs-SZ, after correction for ICV, total brain, cortical gray matter, cerebral white matter, cerebellar gray and white matter, and thalamus volumes were significantly smaller; the cortex was thinner (d < −0.09, q <.05 corrected); and third ventricle was larger (d = +0.15, q <.05 corrected). The findings were not explained by psychopathology in the relatives or control subjects. Conclusions: Despite shared genetic liability, FDRs-SZ and FDRs-BD show a differential pattern of structural brain abnormalities, specifically a divergent effect in ICV. This may imply that the neurodevelopmental trajectories leading to brain anomalies in schizophrenia or bipolar disorder are distinct.

KW - Bipolar disorder

KW - Familial risk

KW - Imaging

KW - Meta-analysis

KW - Neurodevelopment

KW - Schizophrenia

UR - http://www.scopus.com/inward/record.url?scp=85071651930&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85071651930&partnerID=8YFLogxK

U2 - 10.1016/j.biopsych.2019.03.985

DO - 10.1016/j.biopsych.2019.03.985

M3 - Article

C2 - 31443932

AN - SCOPUS:85071651930

VL - 86

SP - 545

EP - 556

JO - Biological Psychiatry

JF - Biological Psychiatry

SN - 0006-3223

IS - 7

ER -