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White matter alterations in Attention-Deficit/Hyperactivity Disorder (ADHD): a systematic review of 129 diffusion imaging studies with meta-analysis

White matter alterations in Attention-Deficit/Hyperactivity Disorder (ADHD): a systematic review of 129 diffusion imaging studies with meta-analysis
White matter alterations in Attention-Deficit/Hyperactivity Disorder (ADHD): a systematic review of 129 diffusion imaging studies with meta-analysis
Aberrant anatomical brain connections in attention-deficit/hyperactivity disorder (ADHD) are reported inconsistently across diffusion weighted imaging (DWI) studies. Based on a pre-registered protocol (Prospero: CRD42021259192), we searched PubMed, Ovid, and Web of Knowledge until 26/03/2022 to conduct a systematic review of DWI studies. We performed a quality assessment based on imaging acquisition, preprocessing, and analysis. Using signed differential mapping, we meta-analyzed a subset of the retrieved studies amenable to quantitative evidence synthesis, i.e., tract-based spatial statistics (TBSS) studies, in individuals of any age and, separately, in children, adults, and high-quality datasets. Finally, we conducted meta-regressions to test the effect of age, sex, and medication-naïvety. We included 129 studies (6739 ADHD participants and 6476 controls), of which 25 TBSS studies provided peak coordinates for case-control differences in fractional anisotropy (FA)(32 datasets) and 18 in mean diffusivity (MD)(23 datasets). The systematic review highlighted white matter alterations (especially reduced FA) in projection, commissural and association pathways of individuals with ADHD, which were associated with symptom severity and cognitive deficits. The meta-analysis showed a consistent reduced FA in the splenium and body of the corpus callosum, extending to the cingulum. Lower FA was related to older age, and case-control differences did not survive in the pediatric meta-analysis. About 68% of studies were of low quality, mainly due to acquisitions with non-isotropic voxels or lack of motion correction; and the sensitivity analysis in high-quality datasets yielded no significant results. Findings suggest prominent alterations in posterior interhemispheric connections subserving cognitive and motor functions affected in ADHD, although these might be influenced by non-optimal acquisition parameters/preprocessing. Absence of findings in children may be related to the late development of callosal fibers, which may enhance case-control differences in adulthood. Clinicodemographic and methodological differences were major barriers to consistency and comparability among studies, and should be addressed in future investigations.
1359-4184
4098–4123
Parlatini, Valeria
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Itahashi, Takashi
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Lee, Yeji
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Liu, Siwei
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Nguyen, Thuan T.
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Aoki, Yuta Y.
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Forkel, Stephanie J.
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Catani, Marco
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Rubia, Katya
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Zhou, Juan H.
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Murphy, Declan G.
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Cortese, Samuele
53d4bf2c-4e0e-4c77-9385-218350560fdb
Parlatini, Valeria
6cdfb200-40ce-43ce-84da-dcb6eba0f67a
Itahashi, Takashi
63261f90-3426-46cd-ac54-db65ed42a522
Lee, Yeji
19b9c7bb-ce72-49c1-8246-2a99de95dcd8
Liu, Siwei
7f8c1bfc-b5d8-49cc-9967-0c0740fa4522
Nguyen, Thuan T.
727dcf98-3b37-4022-a47f-699b0444e8b0
Aoki, Yuta Y.
806ea614-51b3-4018-b68b-d12b7f1487c1
Forkel, Stephanie J.
4ed0aaa6-78dc-4c14-b08f-b3da0171e2d3
Catani, Marco
77eb6337-54aa-417a-9cd2-a32fba812448
Rubia, Katya
5f6c0771-6e32-4924-b3f1-e48ace6de377
Zhou, Juan H.
3e9838c7-1d6c-456f-bbf1-14f8055ef49d
Murphy, Declan G.
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Cortese, Samuele
53d4bf2c-4e0e-4c77-9385-218350560fdb

Parlatini, Valeria, Itahashi, Takashi, Lee, Yeji, Liu, Siwei, Nguyen, Thuan T., Aoki, Yuta Y., Forkel, Stephanie J., Catani, Marco, Rubia, Katya, Zhou, Juan H., Murphy, Declan G. and Cortese, Samuele (2023) White matter alterations in Attention-Deficit/Hyperactivity Disorder (ADHD): a systematic review of 129 diffusion imaging studies with meta-analysis. Molecular Psychiatry, 28, 4098–4123. (doi:10.1038/s41380-023-02173-1).

Record type: Article

Abstract

Aberrant anatomical brain connections in attention-deficit/hyperactivity disorder (ADHD) are reported inconsistently across diffusion weighted imaging (DWI) studies. Based on a pre-registered protocol (Prospero: CRD42021259192), we searched PubMed, Ovid, and Web of Knowledge until 26/03/2022 to conduct a systematic review of DWI studies. We performed a quality assessment based on imaging acquisition, preprocessing, and analysis. Using signed differential mapping, we meta-analyzed a subset of the retrieved studies amenable to quantitative evidence synthesis, i.e., tract-based spatial statistics (TBSS) studies, in individuals of any age and, separately, in children, adults, and high-quality datasets. Finally, we conducted meta-regressions to test the effect of age, sex, and medication-naïvety. We included 129 studies (6739 ADHD participants and 6476 controls), of which 25 TBSS studies provided peak coordinates for case-control differences in fractional anisotropy (FA)(32 datasets) and 18 in mean diffusivity (MD)(23 datasets). The systematic review highlighted white matter alterations (especially reduced FA) in projection, commissural and association pathways of individuals with ADHD, which were associated with symptom severity and cognitive deficits. The meta-analysis showed a consistent reduced FA in the splenium and body of the corpus callosum, extending to the cingulum. Lower FA was related to older age, and case-control differences did not survive in the pediatric meta-analysis. About 68% of studies were of low quality, mainly due to acquisitions with non-isotropic voxels or lack of motion correction; and the sensitivity analysis in high-quality datasets yielded no significant results. Findings suggest prominent alterations in posterior interhemispheric connections subserving cognitive and motor functions affected in ADHD, although these might be influenced by non-optimal acquisition parameters/preprocessing. Absence of findings in children may be related to the late development of callosal fibers, which may enhance case-control differences in adulthood. Clinicodemographic and methodological differences were major barriers to consistency and comparability among studies, and should be addressed in future investigations.

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e-pub ahead of print date: 21 July 2023

Identifiers

Local EPrints ID: 488901
URI: http://eprints.soton.ac.uk/id/eprint/488901
ISSN: 1359-4184
PURE UUID: 12c0335d-c02b-4a15-bf33-cbcd68af1f64
ORCID for Valeria Parlatini: ORCID iD orcid.org/0000-0002-4754-2494
ORCID for Samuele Cortese: ORCID iD orcid.org/0000-0001-5877-8075

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Date deposited: 09 Apr 2024 16:36
Last modified: 10 Sep 2024 02:09

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Contributors

Author: Valeria Parlatini ORCID iD
Author: Takashi Itahashi
Author: Yeji Lee
Author: Siwei Liu
Author: Thuan T. Nguyen
Author: Yuta Y. Aoki
Author: Stephanie J. Forkel
Author: Marco Catani
Author: Katya Rubia
Author: Juan H. Zhou
Author: Declan G. Murphy
Author: Samuele Cortese ORCID iD

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