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November 03, 2020; 95 (18) Article

Developmental neuroplasticity of the white matter connectome in children with perinatal stroke

View ORCID ProfileBrandon T. Craig, Alicia Hilderley, View ORCID ProfileEli Kinney-Lang, Xiangyu Long, View ORCID ProfileHelen L. Carlson, View ORCID ProfileAdam Kirton
First published September 4, 2020, DOI: https://doi.org/10.1212/WNL.0000000000010669
Brandon T. Craig
From the Calgary Pediatric Stroke Program (B.T.C., A.H., E.K.-L., H.L.C., A.K.); and Hotchkiss Brain Institute (B.T.C., A.H., E.K.-L., X.L., H.L.C., A.K.), Alberta Children's Hospital Research Institute (B.T.C., A.H., E.K.-L., X.L., H.L.C., A.K.), and Departments of Pediatrics (H.L.C., A.K.) and Clinical Neuroscience (A.K.), Cumming School of Medicine, University of Calgary, Canada.
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Alicia Hilderley
From the Calgary Pediatric Stroke Program (B.T.C., A.H., E.K.-L., H.L.C., A.K.); and Hotchkiss Brain Institute (B.T.C., A.H., E.K.-L., X.L., H.L.C., A.K.), Alberta Children's Hospital Research Institute (B.T.C., A.H., E.K.-L., X.L., H.L.C., A.K.), and Departments of Pediatrics (H.L.C., A.K.) and Clinical Neuroscience (A.K.), Cumming School of Medicine, University of Calgary, Canada.
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Eli Kinney-Lang
From the Calgary Pediatric Stroke Program (B.T.C., A.H., E.K.-L., H.L.C., A.K.); and Hotchkiss Brain Institute (B.T.C., A.H., E.K.-L., X.L., H.L.C., A.K.), Alberta Children's Hospital Research Institute (B.T.C., A.H., E.K.-L., X.L., H.L.C., A.K.), and Departments of Pediatrics (H.L.C., A.K.) and Clinical Neuroscience (A.K.), Cumming School of Medicine, University of Calgary, Canada.
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Xiangyu Long
From the Calgary Pediatric Stroke Program (B.T.C., A.H., E.K.-L., H.L.C., A.K.); and Hotchkiss Brain Institute (B.T.C., A.H., E.K.-L., X.L., H.L.C., A.K.), Alberta Children's Hospital Research Institute (B.T.C., A.H., E.K.-L., X.L., H.L.C., A.K.), and Departments of Pediatrics (H.L.C., A.K.) and Clinical Neuroscience (A.K.), Cumming School of Medicine, University of Calgary, Canada.
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Helen L. Carlson
From the Calgary Pediatric Stroke Program (B.T.C., A.H., E.K.-L., H.L.C., A.K.); and Hotchkiss Brain Institute (B.T.C., A.H., E.K.-L., X.L., H.L.C., A.K.), Alberta Children's Hospital Research Institute (B.T.C., A.H., E.K.-L., X.L., H.L.C., A.K.), and Departments of Pediatrics (H.L.C., A.K.) and Clinical Neuroscience (A.K.), Cumming School of Medicine, University of Calgary, Canada.
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  • ORCID record for Helen L. Carlson
Adam Kirton
From the Calgary Pediatric Stroke Program (B.T.C., A.H., E.K.-L., H.L.C., A.K.); and Hotchkiss Brain Institute (B.T.C., A.H., E.K.-L., X.L., H.L.C., A.K.), Alberta Children's Hospital Research Institute (B.T.C., A.H., E.K.-L., X.L., H.L.C., A.K.), and Departments of Pediatrics (H.L.C., A.K.) and Clinical Neuroscience (A.K.), Cumming School of Medicine, University of Calgary, Canada.
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Developmental neuroplasticity of the white matter connectome in children with perinatal stroke
Brandon T. Craig, Alicia Hilderley, Eli Kinney-Lang, Xiangyu Long, Helen L. Carlson, Adam Kirton
Neurology Nov 2020, 95 (18) e2476-e2486; DOI: 10.1212/WNL.0000000000010669

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Abstract

Objective To employ diffusion imaging connectome methods to explore network development in the contralesional hemisphere of children with perinatal stroke and its relationship to clinical function. We hypothesized alterations in global efficiency of the intact hemisphere would correlate with clinical disability.

Methods Children with unilateral perinatal arterial (n = 26) or venous (n = 27) stroke and typically developing controls (n = 32) underwent 3T diffusion and T1 anatomical MRI and completed established motor assessments. A validated atlas coregistered to whole-brain tractography for each individual was used to estimate connectivity between 47 regions. Graph theory metrics (assortativity, hierarchical coefficient of regression, global and local efficiency, and small worldness) were calculated for the left hemisphere of controls and the intact contralesioned hemisphere of both stroke groups. Validated clinical motor assessments were then correlated with connectivity outcomes.

Results Global efficiency was higher in arterial strokes compared to venous strokes (p < 0.001) and controls (p < 0.001) and was inversely associated with all motor assessments (all p < 0.012). Additional graph theory metrics including assortativity, hierarchical coefficient of regression, and local efficiency also demonstrated consistent differences in the intact hemisphere associated with clinical function.

Conclusions The structural connectome of the contralesional hemisphere is altered after perinatal stroke and correlates with clinical function. Connectomics represents a powerful tool to understand whole brain developmental plasticity in children with disease-specific cerebral palsy.

Glossary

AAL2=
automated anatomic labeling 2;
ACT=
anatomically constrained tractography;
AHA=
Assisting Hand Assessment;
AIS=
arterial ischemic stroke;
BBTA=
Box and Block Test, affected;
BBTU=
Box and Block Test, unaffected;
CI=
confidence interval;
CSD=
constrained spherical deconvolution;
CST=
corticospinal tract;
dMRI=
diffusion MRI;
FSL=
FMRIB Software Library;
GM=
gray matter;
GRETNA=
graph-theoretical network analysis toolbox;
HCP=
hemiparetic cerebral palsy;
HCR=
hierarchical coefficient of regression;
JTHFA=
Jebsen Taylor Hand Function, affected;
JTHFU=
Jebsen Taylor Hand Function, unaffected;
MUUL=
Melbourne Assessment of Unilateral Upper Limb Function;
PVI=
periventricular venous infarction;
TDC=
typically developing control;
TE=
echo time;
TR=
repetition time;
WM=
white matter

Footnotes

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Received December 6, 2019.
  • Accepted in final form June 3, 2020.
  • © 2020 American Academy of Neurology
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