Cortical and subcortical brain morphometry differences between patients with autism spectrum disorder and healthy individuals across the lifespan: Results from the ENIGMA ASD working group

Daan Van Rooij, Evdokia Anagnostou, Celso Arango, Guillaume Auzias, Marlene Behrmann, Geraldo F. Busatto, Sara Calderoni, Eileen Daly, Christine Deruelle, Adriana Di Martino, Ilan Dinstein, Fabio Luis Souza Duran, Sarah Durston, Christine Ecker, Damien Fair, Jennifer Fedor, Jackie Fitzgerald, Christine M. Freitag, Louise Gallagher, Ilaria GoriShlomi Haar, Liesbeth Hoekstra, Neda Jahanshad, Maria Jalbrzikowski, Joost Janssen, Jason Lerch, Beatriz Luna, Mauricio Moller Martinho, Jane McGrath, Filippo Muratori, Clodagh M. Murphy, Declan G.M. Murphy, Kirsten O'Hearn, Bob Oranje, Mara Parellada, Alessandra Retico, Pedro Rosa, Katya Rubia, Devon Shook, Margot Taylor, Paul M. Thompson, Michela Tosetti, Gregory L. Wallace, Fengfeng Zhou, Jan K. Buitelaar

Research output: Contribution to journalArticle

47 Citations (Scopus)

Abstract

Objective: Neuroimaging studies show structural differences in both cortical and subcortical brain regions in children and adults with autism spectrum disorder (ASD) compared with healthy subjects. Findings are inconsistent, however, and it is unclear how differences develop across the lifespan. The authors investigated brain morphometry differences between individuals with ASD and healthy subjects, crosssectionally across the lifespan, in a large multinational sample from the Enhancing Neuroimaging Genetics Through Meta- Analysis (ENIGMA) ASD working group. Method: The sample comprised 1,571 patients with ASD and 1,651 healthy control subjects (age range, 2-64 years) from 49 participating sites. MRI scans were preprocessed at individual sites with a harmonized protocol based on a validated automated-segmentation software program. Mega-analyses were used to test for case-control differences in subcortical volumes, cortical thickness, and surface area. Development of brain morphometry over the lifespan was modeled using a fractional polynomial approach. Results: The case-control mega-analysis demonstrated that ASD was associated with smaller subcortical volumes of the pallidum, putamen, amygdala, and nucleus accumbens (effect sizes [Cohen'sd],0.13to-0.13), as well as increased cortical thickness in the frontal cortex and decreased thickness in the temporal cortex (effect sizes, 20.21 to 0.20). Analyses of age effects indicate that the development of cortical thickness is altered in ASD, with the largest differences occurring around adolescence.No age-by-ASD interactions were observed in the subcortical partitions. Conclusions: The ENIGMA ASD working group provides the largest study of brain morphometry differences in ASD to date, using a well-established, validated, publicly available analysis pipeline. ASD patients showed altered morphometry in the cognitive and affective parts of the striatum, frontal cortex, and temporal cortex. Complex developmental trajectories were observed for the different regions, with a developmental peak around adolescence. These findings suggest an interplay in the abnormal development of the striatal, frontal, and temporal regions in ASD across the lifespan.

Original languageEnglish (US)
Pages (from-to)359-369
Number of pages11
JournalAmerican Journal of Psychiatry
Volume175
Issue number4
DOIs
StatePublished - Apr 1 2018
Externally publishedYes

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Neuroimaging
Meta-Analysis
Brain
Temporal Lobe
Healthy Volunteers
Frontal Lobe
Autism Spectrum Disorder
Corpus Striatum
Globus Pallidus
Putamen
Nucleus Accumbens
Amygdala
Individuality
Software
Magnetic Resonance Imaging

ASJC Scopus subject areas

  • Psychiatry and Mental health

Cite this

Cortical and subcortical brain morphometry differences between patients with autism spectrum disorder and healthy individuals across the lifespan : Results from the ENIGMA ASD working group. / Van Rooij, Daan; Anagnostou, Evdokia; Arango, Celso; Auzias, Guillaume; Behrmann, Marlene; Busatto, Geraldo F.; Calderoni, Sara; Daly, Eileen; Deruelle, Christine; Di Martino, Adriana; Dinstein, Ilan; Duran, Fabio Luis Souza; Durston, Sarah; Ecker, Christine; Fair, Damien; Fedor, Jennifer; Fitzgerald, Jackie; Freitag, Christine M.; Gallagher, Louise; Gori, Ilaria; Haar, Shlomi; Hoekstra, Liesbeth; Jahanshad, Neda; Jalbrzikowski, Maria; Janssen, Joost; Lerch, Jason; Luna, Beatriz; Martinho, Mauricio Moller; McGrath, Jane; Muratori, Filippo; Murphy, Clodagh M.; Murphy, Declan G.M.; O'Hearn, Kirsten; Oranje, Bob; Parellada, Mara; Retico, Alessandra; Rosa, Pedro; Rubia, Katya; Shook, Devon; Taylor, Margot; Thompson, Paul M.; Tosetti, Michela; Wallace, Gregory L.; Zhou, Fengfeng; Buitelaar, Jan K.

In: American Journal of Psychiatry, Vol. 175, No. 4, 01.04.2018, p. 359-369.

Research output: Contribution to journalArticle

Van Rooij, D, Anagnostou, E, Arango, C, Auzias, G, Behrmann, M, Busatto, GF, Calderoni, S, Daly, E, Deruelle, C, Di Martino, A, Dinstein, I, Duran, FLS, Durston, S, Ecker, C, Fair, D, Fedor, J, Fitzgerald, J, Freitag, CM, Gallagher, L, Gori, I, Haar, S, Hoekstra, L, Jahanshad, N, Jalbrzikowski, M, Janssen, J, Lerch, J, Luna, B, Martinho, MM, McGrath, J, Muratori, F, Murphy, CM, Murphy, DGM, O'Hearn, K, Oranje, B, Parellada, M, Retico, A, Rosa, P, Rubia, K, Shook, D, Taylor, M, Thompson, PM, Tosetti, M, Wallace, GL, Zhou, F & Buitelaar, JK 2018, 'Cortical and subcortical brain morphometry differences between patients with autism spectrum disorder and healthy individuals across the lifespan: Results from the ENIGMA ASD working group', American Journal of Psychiatry, vol. 175, no. 4, pp. 359-369. https://doi.org/10.1176/appi.ajp.2017.17010100
Van Rooij, Daan ; Anagnostou, Evdokia ; Arango, Celso ; Auzias, Guillaume ; Behrmann, Marlene ; Busatto, Geraldo F. ; Calderoni, Sara ; Daly, Eileen ; Deruelle, Christine ; Di Martino, Adriana ; Dinstein, Ilan ; Duran, Fabio Luis Souza ; Durston, Sarah ; Ecker, Christine ; Fair, Damien ; Fedor, Jennifer ; Fitzgerald, Jackie ; Freitag, Christine M. ; Gallagher, Louise ; Gori, Ilaria ; Haar, Shlomi ; Hoekstra, Liesbeth ; Jahanshad, Neda ; Jalbrzikowski, Maria ; Janssen, Joost ; Lerch, Jason ; Luna, Beatriz ; Martinho, Mauricio Moller ; McGrath, Jane ; Muratori, Filippo ; Murphy, Clodagh M. ; Murphy, Declan G.M. ; O'Hearn, Kirsten ; Oranje, Bob ; Parellada, Mara ; Retico, Alessandra ; Rosa, Pedro ; Rubia, Katya ; Shook, Devon ; Taylor, Margot ; Thompson, Paul M. ; Tosetti, Michela ; Wallace, Gregory L. ; Zhou, Fengfeng ; Buitelaar, Jan K. / Cortical and subcortical brain morphometry differences between patients with autism spectrum disorder and healthy individuals across the lifespan : Results from the ENIGMA ASD working group. In: American Journal of Psychiatry. 2018 ; Vol. 175, No. 4. pp. 359-369.
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abstract = "Objective: Neuroimaging studies show structural differences in both cortical and subcortical brain regions in children and adults with autism spectrum disorder (ASD) compared with healthy subjects. Findings are inconsistent, however, and it is unclear how differences develop across the lifespan. The authors investigated brain morphometry differences between individuals with ASD and healthy subjects, crosssectionally across the lifespan, in a large multinational sample from the Enhancing Neuroimaging Genetics Through Meta- Analysis (ENIGMA) ASD working group. Method: The sample comprised 1,571 patients with ASD and 1,651 healthy control subjects (age range, 2-64 years) from 49 participating sites. MRI scans were preprocessed at individual sites with a harmonized protocol based on a validated automated-segmentation software program. Mega-analyses were used to test for case-control differences in subcortical volumes, cortical thickness, and surface area. Development of brain morphometry over the lifespan was modeled using a fractional polynomial approach. Results: The case-control mega-analysis demonstrated that ASD was associated with smaller subcortical volumes of the pallidum, putamen, amygdala, and nucleus accumbens (effect sizes [Cohen'sd],0.13to-0.13), as well as increased cortical thickness in the frontal cortex and decreased thickness in the temporal cortex (effect sizes, 20.21 to 0.20). Analyses of age effects indicate that the development of cortical thickness is altered in ASD, with the largest differences occurring around adolescence.No age-by-ASD interactions were observed in the subcortical partitions. Conclusions: The ENIGMA ASD working group provides the largest study of brain morphometry differences in ASD to date, using a well-established, validated, publicly available analysis pipeline. ASD patients showed altered morphometry in the cognitive and affective parts of the striatum, frontal cortex, and temporal cortex. Complex developmental trajectories were observed for the different regions, with a developmental peak around adolescence. These findings suggest an interplay in the abnormal development of the striatal, frontal, and temporal regions in ASD across the lifespan.",
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T1 - Cortical and subcortical brain morphometry differences between patients with autism spectrum disorder and healthy individuals across the lifespan

T2 - Results from the ENIGMA ASD working group

AU - Van Rooij, Daan

AU - Anagnostou, Evdokia

AU - Arango, Celso

AU - Auzias, Guillaume

AU - Behrmann, Marlene

AU - Busatto, Geraldo F.

AU - Calderoni, Sara

AU - Daly, Eileen

AU - Deruelle, Christine

AU - Di Martino, Adriana

AU - Dinstein, Ilan

AU - Duran, Fabio Luis Souza

AU - Durston, Sarah

AU - Ecker, Christine

AU - Fair, Damien

AU - Fedor, Jennifer

AU - Fitzgerald, Jackie

AU - Freitag, Christine M.

AU - Gallagher, Louise

AU - Gori, Ilaria

AU - Haar, Shlomi

AU - Hoekstra, Liesbeth

AU - Jahanshad, Neda

AU - Jalbrzikowski, Maria

AU - Janssen, Joost

AU - Lerch, Jason

AU - Luna, Beatriz

AU - Martinho, Mauricio Moller

AU - McGrath, Jane

AU - Muratori, Filippo

AU - Murphy, Clodagh M.

AU - Murphy, Declan G.M.

AU - O'Hearn, Kirsten

AU - Oranje, Bob

AU - Parellada, Mara

AU - Retico, Alessandra

AU - Rosa, Pedro

AU - Rubia, Katya

AU - Shook, Devon

AU - Taylor, Margot

AU - Thompson, Paul M.

AU - Tosetti, Michela

AU - Wallace, Gregory L.

AU - Zhou, Fengfeng

AU - Buitelaar, Jan K.

PY - 2018/4/1

Y1 - 2018/4/1

N2 - Objective: Neuroimaging studies show structural differences in both cortical and subcortical brain regions in children and adults with autism spectrum disorder (ASD) compared with healthy subjects. Findings are inconsistent, however, and it is unclear how differences develop across the lifespan. The authors investigated brain morphometry differences between individuals with ASD and healthy subjects, crosssectionally across the lifespan, in a large multinational sample from the Enhancing Neuroimaging Genetics Through Meta- Analysis (ENIGMA) ASD working group. Method: The sample comprised 1,571 patients with ASD and 1,651 healthy control subjects (age range, 2-64 years) from 49 participating sites. MRI scans were preprocessed at individual sites with a harmonized protocol based on a validated automated-segmentation software program. Mega-analyses were used to test for case-control differences in subcortical volumes, cortical thickness, and surface area. Development of brain morphometry over the lifespan was modeled using a fractional polynomial approach. Results: The case-control mega-analysis demonstrated that ASD was associated with smaller subcortical volumes of the pallidum, putamen, amygdala, and nucleus accumbens (effect sizes [Cohen'sd],0.13to-0.13), as well as increased cortical thickness in the frontal cortex and decreased thickness in the temporal cortex (effect sizes, 20.21 to 0.20). Analyses of age effects indicate that the development of cortical thickness is altered in ASD, with the largest differences occurring around adolescence.No age-by-ASD interactions were observed in the subcortical partitions. Conclusions: The ENIGMA ASD working group provides the largest study of brain morphometry differences in ASD to date, using a well-established, validated, publicly available analysis pipeline. ASD patients showed altered morphometry in the cognitive and affective parts of the striatum, frontal cortex, and temporal cortex. Complex developmental trajectories were observed for the different regions, with a developmental peak around adolescence. These findings suggest an interplay in the abnormal development of the striatal, frontal, and temporal regions in ASD across the lifespan.

AB - Objective: Neuroimaging studies show structural differences in both cortical and subcortical brain regions in children and adults with autism spectrum disorder (ASD) compared with healthy subjects. Findings are inconsistent, however, and it is unclear how differences develop across the lifespan. The authors investigated brain morphometry differences between individuals with ASD and healthy subjects, crosssectionally across the lifespan, in a large multinational sample from the Enhancing Neuroimaging Genetics Through Meta- Analysis (ENIGMA) ASD working group. Method: The sample comprised 1,571 patients with ASD and 1,651 healthy control subjects (age range, 2-64 years) from 49 participating sites. MRI scans were preprocessed at individual sites with a harmonized protocol based on a validated automated-segmentation software program. Mega-analyses were used to test for case-control differences in subcortical volumes, cortical thickness, and surface area. Development of brain morphometry over the lifespan was modeled using a fractional polynomial approach. Results: The case-control mega-analysis demonstrated that ASD was associated with smaller subcortical volumes of the pallidum, putamen, amygdala, and nucleus accumbens (effect sizes [Cohen'sd],0.13to-0.13), as well as increased cortical thickness in the frontal cortex and decreased thickness in the temporal cortex (effect sizes, 20.21 to 0.20). Analyses of age effects indicate that the development of cortical thickness is altered in ASD, with the largest differences occurring around adolescence.No age-by-ASD interactions were observed in the subcortical partitions. Conclusions: The ENIGMA ASD working group provides the largest study of brain morphometry differences in ASD to date, using a well-established, validated, publicly available analysis pipeline. ASD patients showed altered morphometry in the cognitive and affective parts of the striatum, frontal cortex, and temporal cortex. Complex developmental trajectories were observed for the different regions, with a developmental peak around adolescence. These findings suggest an interplay in the abnormal development of the striatal, frontal, and temporal regions in ASD across the lifespan.

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