Brain network reorganisation and spatial lesion distribution in systemic lupus erythematosus

Maria del C. Valdés Hernández; Keith Smith; Mark E. Bastin; E. Nicole Amft; Stuart H. Ralston; Joanna M. Wardlaw; Stewart J. Wiseman

doi:10.1177/0961203320979045

Brain network reorganisation and spatial lesion distribution in systemic lupus erythematosus

Maria del C. Valdés Hernández, Keith Smith, Mark E. Bastin, E. Nicole Amft, Stuart H. Ralston, Joanna M. Wardlaw, Stewart J. Wiseman^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

6 Citations (Scopus)

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Abstract

Objective
This work investigates network organisation of brain structural connectivity in systemic lupus erythematosus (SLE) relative to healthy controls and its putative association with lesion distribution and disease indicators.

Methods
White matter hyperintensity (WMH) segmentation and connectomics were performed in 47 patients with SLE and 47 healthy age-matched controls from structural and diffusion MRI data. Network nodes were divided into hierarchical tiers based on numbers of connections. Results were compared between patients and controls to assess for differences in brain network organisation. Voxel-based analyses of the spatial distribution of WMH in relation to network measures and SLE disease indicators were conducted.

Results
Despite inter-individual differences in brain network organization observed across the study sample, the connectome networks of SLE patients had larger proportion of connections in the peripheral nodes. SLE patients had statistically larger numbers of links in their networks with generally larger fractional anisotropy weights (i.e. a measure of white matter integrity) and less tendency to aggregate than those of healthy controls. The voxels exhibiting connectomic differences were coincident with WMH clusters, particularly the left hemisphere’s intersection between the anterior limb of the internal and external capsules. Moreover, these voxels also associated more strongly with disease indicators.

Conclusion
Our results indicate network differences reflective of compensatory reorganization of the neural circuits, reflecting adaptive or extended neuroplasticity in SLE.

Original language	English
Pages (from-to)	285-298
Number of pages	14
Journal	Lupus
Volume	30
Issue number	2
Early online date	13 Dec 2020
DOIs	https://doi.org/10.1177/0961203320979045
Publication status	Published - 28 Feb 2021
Externally published	Yes

Funding

We acknowledge support from the Scottish Lupus Exchange registry. The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by Row Fogo Charitable Trust [BROD.FID3668413 to MVH]; the European Union Horizon 2020 [PHC-03-15, 666881, ‘SVDs@Target’ to JMW]; the Stroke Association [SA PDF 18\100026 to SJW]; Lupus UK and the University of Edinburgh. Image acquisition and data processing for the control subjects was funded by the National Institutes of Health [R01 EB004155]. This work was also supported by the UK Dementia Research Institute which receives its funding from DRI Ltd, funded by the UK Medical Research Council, Alzheimer’s Society and Alzheimer’s Research UK. KMS was supported by Health Data Research UK, an initiative funded by UK Research and Innovation Councils, National Institute for Health Research (England) and the UK devolved administrations, and leading medical research charities. Acknowledgements

Keywords

connectome
network analysis
SLE

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10.1177/0961203320979045Licence: CC BY 4.0

Valdes-Hernandez-etal-Lupus-2020-Brain-network-reorganisation-and-spatial-lesion-distribution-in-systemic-lupus-erythematosusFinal published version, 1 MBLicence: CC BY 4.0

Cite this

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title = "Brain network reorganisation and spatial lesion distribution in systemic lupus erythematosus",

abstract = "ObjectiveThis work investigates network organisation of brain structural connectivity in systemic lupus erythematosus (SLE) relative to healthy controls and its putative association with lesion distribution and disease indicators.MethodsWhite matter hyperintensity (WMH) segmentation and connectomics were performed in 47 patients with SLE and 47 healthy age-matched controls from structural and diffusion MRI data. Network nodes were divided into hierarchical tiers based on numbers of connections. Results were compared between patients and controls to assess for differences in brain network organisation. Voxel-based analyses of the spatial distribution of WMH in relation to network measures and SLE disease indicators were conducted.ResultsDespite inter-individual differences in brain network organization observed across the study sample, the connectome networks of SLE patients had larger proportion of connections in the peripheral nodes. SLE patients had statistically larger numbers of links in their networks with generally larger fractional anisotropy weights (i.e. a measure of white matter integrity) and less tendency to aggregate than those of healthy controls. The voxels exhibiting connectomic differences were coincident with WMH clusters, particularly the left hemisphere{\textquoteright}s intersection between the anterior limb of the internal and external capsules. Moreover, these voxels also associated more strongly with disease indicators.ConclusionOur results indicate network differences reflective of compensatory reorganization of the neural circuits, reflecting adaptive or extended neuroplasticity in SLE.",

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author = "{Vald{\'e}s Hern{\'a}ndez}, {Maria del C.} and Keith Smith and Bastin, {Mark E.} and {Nicole Amft}, E. and Ralston, {Stuart H.} and Wardlaw, {Joanna M.} and Wiseman, {Stewart J.}",

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T1 - Brain network reorganisation and spatial lesion distribution in systemic lupus erythematosus

AU - Valdés Hernández, Maria del C.

AU - Smith, Keith

AU - Bastin, Mark E.

AU - Nicole Amft, E.

AU - Ralston, Stuart H.

AU - Wardlaw, Joanna M.

AU - Wiseman, Stewart J.

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N2 - ObjectiveThis work investigates network organisation of brain structural connectivity in systemic lupus erythematosus (SLE) relative to healthy controls and its putative association with lesion distribution and disease indicators.MethodsWhite matter hyperintensity (WMH) segmentation and connectomics were performed in 47 patients with SLE and 47 healthy age-matched controls from structural and diffusion MRI data. Network nodes were divided into hierarchical tiers based on numbers of connections. Results were compared between patients and controls to assess for differences in brain network organisation. Voxel-based analyses of the spatial distribution of WMH in relation to network measures and SLE disease indicators were conducted.ResultsDespite inter-individual differences in brain network organization observed across the study sample, the connectome networks of SLE patients had larger proportion of connections in the peripheral nodes. SLE patients had statistically larger numbers of links in their networks with generally larger fractional anisotropy weights (i.e. a measure of white matter integrity) and less tendency to aggregate than those of healthy controls. The voxels exhibiting connectomic differences were coincident with WMH clusters, particularly the left hemisphere’s intersection between the anterior limb of the internal and external capsules. Moreover, these voxels also associated more strongly with disease indicators.ConclusionOur results indicate network differences reflective of compensatory reorganization of the neural circuits, reflecting adaptive or extended neuroplasticity in SLE.

AB - ObjectiveThis work investigates network organisation of brain structural connectivity in systemic lupus erythematosus (SLE) relative to healthy controls and its putative association with lesion distribution and disease indicators.MethodsWhite matter hyperintensity (WMH) segmentation and connectomics were performed in 47 patients with SLE and 47 healthy age-matched controls from structural and diffusion MRI data. Network nodes were divided into hierarchical tiers based on numbers of connections. Results were compared between patients and controls to assess for differences in brain network organisation. Voxel-based analyses of the spatial distribution of WMH in relation to network measures and SLE disease indicators were conducted.ResultsDespite inter-individual differences in brain network organization observed across the study sample, the connectome networks of SLE patients had larger proportion of connections in the peripheral nodes. SLE patients had statistically larger numbers of links in their networks with generally larger fractional anisotropy weights (i.e. a measure of white matter integrity) and less tendency to aggregate than those of healthy controls. The voxels exhibiting connectomic differences were coincident with WMH clusters, particularly the left hemisphere’s intersection between the anterior limb of the internal and external capsules. Moreover, these voxels also associated more strongly with disease indicators.ConclusionOur results indicate network differences reflective of compensatory reorganization of the neural circuits, reflecting adaptive or extended neuroplasticity in SLE.

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KW - network analysis

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Brain network reorganisation and spatial lesion distribution in systemic lupus erythematosus

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Keywords

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