Left hemisphere structural connectivity abnormality in pediatric hydrocephalus patients following surgery

Neuroimaging research in surgically treated pediatric hydrocephalus patients remains challenging due to the artifact caused by programmable shunt. Our previous study has demonstrated significant alterations in the whole brain white matter structural connectivity based on diffusion tensor imaging (DT...

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Main Authors: Weihong Yuan, Artur Meller, Joshua S. Shimony, Tiffany Nash, Blaise V. Jones, Scott K. Holland, Mekibib Altaye, Holly Barnard, Jannel Phillips, Stephanie Powell, Robert C. McKinstry, David D. Limbrick, Akila Rajagopal, Francesco T. Mangano
Format: Article
Language:English
Published: Elsevier 2016-01-01
Series:NeuroImage: Clinical
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2213158216301619
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language English
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author Weihong Yuan
Artur Meller
Joshua S. Shimony
Tiffany Nash
Blaise V. Jones
Scott K. Holland
Mekibib Altaye
Holly Barnard
Jannel Phillips
Stephanie Powell
Robert C. McKinstry
David D. Limbrick
Akila Rajagopal
Francesco T. Mangano
spellingShingle Weihong Yuan
Artur Meller
Joshua S. Shimony
Tiffany Nash
Blaise V. Jones
Scott K. Holland
Mekibib Altaye
Holly Barnard
Jannel Phillips
Stephanie Powell
Robert C. McKinstry
David D. Limbrick
Akila Rajagopal
Francesco T. Mangano
Left hemisphere structural connectivity abnormality in pediatric hydrocephalus patients following surgery
NeuroImage: Clinical
Diffusion tensor imaging
Graph theoretical analysis
Left hemisphere
Pediatric hydrocephalus
Small-worldness
author_facet Weihong Yuan
Artur Meller
Joshua S. Shimony
Tiffany Nash
Blaise V. Jones
Scott K. Holland
Mekibib Altaye
Holly Barnard
Jannel Phillips
Stephanie Powell
Robert C. McKinstry
David D. Limbrick
Akila Rajagopal
Francesco T. Mangano
author_sort Weihong Yuan
title Left hemisphere structural connectivity abnormality in pediatric hydrocephalus patients following surgery
title_short Left hemisphere structural connectivity abnormality in pediatric hydrocephalus patients following surgery
title_full Left hemisphere structural connectivity abnormality in pediatric hydrocephalus patients following surgery
title_fullStr Left hemisphere structural connectivity abnormality in pediatric hydrocephalus patients following surgery
title_full_unstemmed Left hemisphere structural connectivity abnormality in pediatric hydrocephalus patients following surgery
title_sort left hemisphere structural connectivity abnormality in pediatric hydrocephalus patients following surgery
publisher Elsevier
series NeuroImage: Clinical
issn 2213-1582
publishDate 2016-01-01
description Neuroimaging research in surgically treated pediatric hydrocephalus patients remains challenging due to the artifact caused by programmable shunt. Our previous study has demonstrated significant alterations in the whole brain white matter structural connectivity based on diffusion tensor imaging (DTI) and graph theoretical analysis in children with hydrocephalus prior to surgery or in surgically treated children without programmable shunts. This study seeks to investigate the impact of brain injury on the topological features in the left hemisphere, contratelateral to the shunt placement, which will avoid the influence of shunt artifacts and makes further group comparisons feasible for children with programmable shunt valves. Three groups of children (34 in the control group, 12 in the 3-month post-surgery group, and 24 in the 12-month post-surgery group, age between 1 and 18 years) were included in the study. The structural connectivity data processing and analysis were performed based on DTI and graph theoretical analysis. Specific procedures were revised to include only left brain imaging data in normalization, parcellation, and fiber counting from DTI tractography. Our results showed that, when compared to controls, children with hydrocephalus in both the 3-month and 12-month post-surgery groups had significantly lower normalized clustering coefficient, lower small-worldness, and higher global efficiency (all p < 0.05, corrected). At a regional level, both patient groups showed significant alteration in one or more regional connectivity measures in a series of brain regions in the left hemisphere (8 and 10 regions in the 3-month post-surgery and the 12-month post-surgery group, respectively, all p < 0.05, corrected). No significant correlation was found between any of the global or regional measures and the contemporaneous neuropsychological outcomes [the General Adaptive Composite (GAC) from the Adaptive Behavior Assessment System, Second Edition (ABAS-II)]. However, one global network measure (global efficiency) and two regional network measures in the insula (local efficiency and between centrality) tested at 3-month post-surgery were found to correlate with GAC score tested at 12-month post-surgery with statistical significance (all p < 0.05, corrected). Our data showed that the structural connectivity analysis based on DTI and graph theory was sensitive in detecting both global and regional network abnormality when the analysis was conducted in the left hemisphere only. This approach provides a new avenue enabling the application of advanced neuroimaging analysis methods in quantifying brain damage in children with hydrocephalus surgically treated with programmable shunts.
topic Diffusion tensor imaging
Graph theoretical analysis
Left hemisphere
Pediatric hydrocephalus
Small-worldness
url http://www.sciencedirect.com/science/article/pii/S2213158216301619
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spelling doaj-206b47c41360440fa48aa464bcacaee12020-11-25T00:20:18ZengElsevierNeuroImage: Clinical2213-15822016-01-0112C63163910.1016/j.nicl.2016.09.003Left hemisphere structural connectivity abnormality in pediatric hydrocephalus patients following surgeryWeihong Yuan0Artur Meller1Joshua S. Shimony2Tiffany Nash3Blaise V. Jones4Scott K. Holland5Mekibib Altaye6Holly Barnard7Jannel Phillips8Stephanie Powell9Robert C. McKinstry10David D. Limbrick11Akila Rajagopal12Francesco T. Mangano13Department of Radiology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, United StatesDepartment of Radiology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, United StatesMallinckrodt Institute of Radiology, Washington University School of Medicine, Saint Louis, MO, United StatesDepartment of Radiology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, United StatesDepartment of Radiology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, United StatesDepartment of Radiology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, United StatesDivision of Biostatistics and Epidemiology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, United StatesDivision of Developmental and Behavioral Pediatrics – Psychology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, United StatesDivision of Developmental and Behavioral Pediatrics – Psychology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, United StatesDepartment of Neurology, Washington University School of Medicine, Saint Louis, MO, United StatesMallinckrodt Institute of Radiology, Washington University School of Medicine, Saint Louis, MO, United StatesDepartment of Neurological Surgery, Washington University School of Medicine, Saint Louis, MO, United StatesDepartment of Radiology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, United StatesDivision of Pediatric Neurosurgery, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, United StatesNeuroimaging research in surgically treated pediatric hydrocephalus patients remains challenging due to the artifact caused by programmable shunt. Our previous study has demonstrated significant alterations in the whole brain white matter structural connectivity based on diffusion tensor imaging (DTI) and graph theoretical analysis in children with hydrocephalus prior to surgery or in surgically treated children without programmable shunts. This study seeks to investigate the impact of brain injury on the topological features in the left hemisphere, contratelateral to the shunt placement, which will avoid the influence of shunt artifacts and makes further group comparisons feasible for children with programmable shunt valves. Three groups of children (34 in the control group, 12 in the 3-month post-surgery group, and 24 in the 12-month post-surgery group, age between 1 and 18 years) were included in the study. The structural connectivity data processing and analysis were performed based on DTI and graph theoretical analysis. Specific procedures were revised to include only left brain imaging data in normalization, parcellation, and fiber counting from DTI tractography. Our results showed that, when compared to controls, children with hydrocephalus in both the 3-month and 12-month post-surgery groups had significantly lower normalized clustering coefficient, lower small-worldness, and higher global efficiency (all p < 0.05, corrected). At a regional level, both patient groups showed significant alteration in one or more regional connectivity measures in a series of brain regions in the left hemisphere (8 and 10 regions in the 3-month post-surgery and the 12-month post-surgery group, respectively, all p < 0.05, corrected). No significant correlation was found between any of the global or regional measures and the contemporaneous neuropsychological outcomes [the General Adaptive Composite (GAC) from the Adaptive Behavior Assessment System, Second Edition (ABAS-II)]. However, one global network measure (global efficiency) and two regional network measures in the insula (local efficiency and between centrality) tested at 3-month post-surgery were found to correlate with GAC score tested at 12-month post-surgery with statistical significance (all p < 0.05, corrected). Our data showed that the structural connectivity analysis based on DTI and graph theory was sensitive in detecting both global and regional network abnormality when the analysis was conducted in the left hemisphere only. This approach provides a new avenue enabling the application of advanced neuroimaging analysis methods in quantifying brain damage in children with hydrocephalus surgically treated with programmable shunts.http://www.sciencedirect.com/science/article/pii/S2213158216301619Diffusion tensor imagingGraph theoretical analysisLeft hemispherePediatric hydrocephalusSmall-worldness