Alterations in Functional Connectomics Associated with Neurocognitive Changes following Glioma Resection

Kyle R. Noll; Henry S. Chen; Jeffrey S. Wefel; Vinodh A. Kumar; Ping Hou; Sherise D. Ferguson; Ganesh Rao; Jason M. Johnson; Donald F. Schomer; Dima Suki; Sujit S. Prabhu; Ho Ling Liu

doi:10.1093/neuros/nyaa453

Alterations in Functional Connectomics Associated with Neurocognitive Changes following Glioma Resection

Kyle R. Noll, Henry S. Chen, Jeffrey S. Wefel, Vinodh A. Kumar, Ping Hou, Sherise D. Ferguson, Ganesh Rao, Jason M. Johnson, Donald F. Schomer, Dima Suki, Sujit S. Prabhu, Ho Ling Liu

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

9 Scopus citations

Abstract

BACKGROUND: Decline in neurocognitive functioning (NCF) often occurs following brain tumor resection. Functional connectomics have shown how neurologic insults disrupt cerebral networks underlying NCF, though studies involving patients with brain tumors are lacking. OBJECTIVE: To investigate the impact of brain tumor resection upon the connectome and relationships with NCF outcome in the early postoperative period. METHODS: A total of 15 right-handed adults with left perisylvian glioma underwent resting-state functional magnetic resonance imaging (rs-fMRI) and neuropsychological assessment before and after awake tumor resection. Graph theoretical analysis was applied to rs-fMRI connectivity matrices to calculate network properties. Network properties and NCF measures were compared across the pre- to postoperative periods with matched pairs Wilcoxon signed-rank tests. Associations between pre- to postoperative change in network and NCF measures were determined with Spearman rank-order correlations (ρ). RESULTS: A majority of the sample showed postoperative decline on 1 or more NCF measures. Significant postoperative NCF decline was found across measures of verbal memory, processing speed, executive functioning, receptive language, and a composite index. Regarding connectomic properties, betweenness centrality and assortativity were significantly smaller postoperatively, and reductions in these measures were associated with better NCF outcomes. Significant inverse associations (ρ = -.51 to -.78, all P <. 05) were observed between change in language, executive functioning, and learning and memory, and alterations in segregation, centrality, and resilience network properties. CONCLUSION: Decline in NCF was common shortly following resection of glioma involving eloquent brain regions, most frequently in verbal learning/memory and executive functioning. Better postoperative outcomes accompanied reductions in centrality and resilience connectomic measures.

Original language	English (US)
Pages (from-to)	544-551
Number of pages	8
Journal	Neurosurgery
Volume	88
Issue number	3
DOIs	https://doi.org/10.1093/neuros/nyaa453
State	Published - Mar 1 2021

Keywords

Brain tumor
Connectomics
Functional imaging
Glioma
Neurocognitive function

ASJC Scopus subject areas

Surgery
Clinical Neurology

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10.1093/neuros/nyaa453

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@article{1883eded9ff54ffd82b4a20c1932b461,

title = "Alterations in Functional Connectomics Associated with Neurocognitive Changes following Glioma Resection",

abstract = "BACKGROUND: Decline in neurocognitive functioning (NCF) often occurs following brain tumor resection. Functional connectomics have shown how neurologic insults disrupt cerebral networks underlying NCF, though studies involving patients with brain tumors are lacking. OBJECTIVE: To investigate the impact of brain tumor resection upon the connectome and relationships with NCF outcome in the early postoperative period. METHODS: A total of 15 right-handed adults with left perisylvian glioma underwent resting-state functional magnetic resonance imaging (rs-fMRI) and neuropsychological assessment before and after awake tumor resection. Graph theoretical analysis was applied to rs-fMRI connectivity matrices to calculate network properties. Network properties and NCF measures were compared across the pre- to postoperative periods with matched pairs Wilcoxon signed-rank tests. Associations between pre- to postoperative change in network and NCF measures were determined with Spearman rank-order correlations (ρ). RESULTS: A majority of the sample showed postoperative decline on 1 or more NCF measures. Significant postoperative NCF decline was found across measures of verbal memory, processing speed, executive functioning, receptive language, and a composite index. Regarding connectomic properties, betweenness centrality and assortativity were significantly smaller postoperatively, and reductions in these measures were associated with better NCF outcomes. Significant inverse associations (ρ = -.51 to -.78, all P <. 05) were observed between change in language, executive functioning, and learning and memory, and alterations in segregation, centrality, and resilience network properties. CONCLUSION: Decline in NCF was common shortly following resection of glioma involving eloquent brain regions, most frequently in verbal learning/memory and executive functioning. Better postoperative outcomes accompanied reductions in centrality and resilience connectomic measures.",

keywords = "Brain tumor, Connectomics, Functional imaging, Glioma, Neurocognitive function",

author = "Noll, {Kyle R.} and Chen, {Henry S.} and Wefel, {Jeffrey S.} and Kumar, {Vinodh A.} and Ping Hou and Ferguson, {Sherise D.} and Ganesh Rao and Johnson, {Jason M.} and Schomer, {Donald F.} and Dima Suki and Prabhu, {Sujit S.} and Liu, {Ho Ling}",

note = "Publisher Copyright: Copyright {\textcopyright} 2020 by the Congress of Neurological Surgeons.",

year = "2021",

month = mar,

day = "1",

doi = "10.1093/neuros/nyaa453",

language = "English (US)",

volume = "88",

pages = "544--551",

journal = "Neurosurgery",

issn = "0148-396X",

publisher = "Lippincott Williams and Wilkins Ltd.",

number = "3",

}

TY - JOUR

T1 - Alterations in Functional Connectomics Associated with Neurocognitive Changes following Glioma Resection

AU - Noll, Kyle R.

AU - Chen, Henry S.

AU - Wefel, Jeffrey S.

AU - Kumar, Vinodh A.

AU - Hou, Ping

AU - Ferguson, Sherise D.

AU - Rao, Ganesh

AU - Johnson, Jason M.

AU - Schomer, Donald F.

AU - Suki, Dima

AU - Prabhu, Sujit S.

AU - Liu, Ho Ling

PY - 2021/3/1

Y1 - 2021/3/1

N2 - BACKGROUND: Decline in neurocognitive functioning (NCF) often occurs following brain tumor resection. Functional connectomics have shown how neurologic insults disrupt cerebral networks underlying NCF, though studies involving patients with brain tumors are lacking. OBJECTIVE: To investigate the impact of brain tumor resection upon the connectome and relationships with NCF outcome in the early postoperative period. METHODS: A total of 15 right-handed adults with left perisylvian glioma underwent resting-state functional magnetic resonance imaging (rs-fMRI) and neuropsychological assessment before and after awake tumor resection. Graph theoretical analysis was applied to rs-fMRI connectivity matrices to calculate network properties. Network properties and NCF measures were compared across the pre- to postoperative periods with matched pairs Wilcoxon signed-rank tests. Associations between pre- to postoperative change in network and NCF measures were determined with Spearman rank-order correlations (ρ). RESULTS: A majority of the sample showed postoperative decline on 1 or more NCF measures. Significant postoperative NCF decline was found across measures of verbal memory, processing speed, executive functioning, receptive language, and a composite index. Regarding connectomic properties, betweenness centrality and assortativity were significantly smaller postoperatively, and reductions in these measures were associated with better NCF outcomes. Significant inverse associations (ρ = -.51 to -.78, all P <. 05) were observed between change in language, executive functioning, and learning and memory, and alterations in segregation, centrality, and resilience network properties. CONCLUSION: Decline in NCF was common shortly following resection of glioma involving eloquent brain regions, most frequently in verbal learning/memory and executive functioning. Better postoperative outcomes accompanied reductions in centrality and resilience connectomic measures.

AB - BACKGROUND: Decline in neurocognitive functioning (NCF) often occurs following brain tumor resection. Functional connectomics have shown how neurologic insults disrupt cerebral networks underlying NCF, though studies involving patients with brain tumors are lacking. OBJECTIVE: To investigate the impact of brain tumor resection upon the connectome and relationships with NCF outcome in the early postoperative period. METHODS: A total of 15 right-handed adults with left perisylvian glioma underwent resting-state functional magnetic resonance imaging (rs-fMRI) and neuropsychological assessment before and after awake tumor resection. Graph theoretical analysis was applied to rs-fMRI connectivity matrices to calculate network properties. Network properties and NCF measures were compared across the pre- to postoperative periods with matched pairs Wilcoxon signed-rank tests. Associations between pre- to postoperative change in network and NCF measures were determined with Spearman rank-order correlations (ρ). RESULTS: A majority of the sample showed postoperative decline on 1 or more NCF measures. Significant postoperative NCF decline was found across measures of verbal memory, processing speed, executive functioning, receptive language, and a composite index. Regarding connectomic properties, betweenness centrality and assortativity were significantly smaller postoperatively, and reductions in these measures were associated with better NCF outcomes. Significant inverse associations (ρ = -.51 to -.78, all P <. 05) were observed between change in language, executive functioning, and learning and memory, and alterations in segregation, centrality, and resilience network properties. CONCLUSION: Decline in NCF was common shortly following resection of glioma involving eloquent brain regions, most frequently in verbal learning/memory and executive functioning. Better postoperative outcomes accompanied reductions in centrality and resilience connectomic measures.

KW - Brain tumor

KW - Connectomics

KW - Functional imaging

KW - Glioma

KW - Neurocognitive function

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UR - http://www.scopus.com/inward/citedby.url?scp=85102153785&partnerID=8YFLogxK

U2 - 10.1093/neuros/nyaa453

DO - 10.1093/neuros/nyaa453

M3 - Article

C2 - 33080024

AN - SCOPUS:85102153785

SN - 0148-396X

VL - 88

SP - 544

EP - 551

JO - Neurosurgery

JF - Neurosurgery

IS - 3

ER -

Alterations in Functional Connectomics Associated with Neurocognitive Changes following Glioma Resection

Abstract

Keywords

ASJC Scopus subject areas

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