Bold coupling between lesioned and healthy brain is associated with glioma patients’ recovery

Rafael Romero-Garcia; Michael G. Hart; Richard A.I. Bethlehem; Ayan Mandal; Moataz Assem; Benedicto Crespo-Facorro; Juan Manuel Gorriz; Gladstone Austin Amos Burke; Stephen J. Price; Thomas Santarius; Yaara Erez; John Suckling

doi:10.3390/cancers13195008

Bold coupling between lesioned and healthy brain is associated with glioma patients’ recovery

Rafael Romero-Garcia^*, Michael G. Hart, Richard A.I. Bethlehem, Ayan Mandal, Moataz Assem, Benedicto Crespo-Facorro, Juan Manuel Gorriz, Gladstone Austin Amos Burke, Stephen J. Price, Thomas Santarius, Yaara Erez, John Suckling

^*Corresponding author for this work

Cancer and Genomic Sciences

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

15 Downloads (Pure)

Abstract

Predicting functional outcomes after surgery and early adjuvant treatment is difficult due to the complex, extended, interlocking brain networks that underpin cognition. The aim of this study was to test glioma functional interactions with the rest of the brain, thereby identifying the risk factors of cognitive recovery or deterioration. Seventeen patients with diffuse non-enhancing glioma (aged 22–56 years) were longitudinally MRI scanned and cognitively assessed before and after surgery and during a 12-month recovery period (55 MRI scans in total after exclusions). We initially found, and then replicated in an independent dataset, that the spatial correlation pattern between regional and global BOLD signals (also known as global signal topography) was associated with tumour occurrence. We then estimated the coupling between the BOLD signal from within the tumour and the signal extracted from different brain tissues. We observed that the normative global signal topography is reorganised in glioma patients during the recovery period. Moreover, we found that the BOLD signal within the tumour and lesioned brain was coupled with the global signal and that this coupling was associated with cognitive recovery. Nevertheless, patients did not show any apparent disruption of functional connectivity within canonical functional networks. Understanding how tumour infiltration and coupling are related to patients’ recovery represents a major step forward in prognostic development.

Original language	English
Article number	5008
Number of pages	19
Journal	Cancers
Volume	13
Issue number	19
DOIs	https://doi.org/10.3390/cancers13195008
Publication status	Published - 6 Oct 2021

Bibliographical note

Funding Information:
This research was supported by the Guarantors of Brain, Cancer Research UK Cambridge Centre, The Brain Tumour Charity and the EMERGIA Junta de Andalucia program. Y.E. is funded by a Royal Society Dorothy Hodgkin Research Fellowship (DHF130100). JMG is funded by the Ministerio de Ciencia e Innovación (España)/FEDER under the RTI2018-098913-B100 project, by the Consejería de Economía, Innovación, Ciencia y Empleo (Junta de Andalucía) and FEDER under CV20-45250, A-TIC-080-UGR18, B-TIC-586-UGR20 and P20-00525 projects. MA was funded by a Cambridge Trust—Yousef Jameel Scholarship. This research was also supported by the NIHR Cambridge Biomedical Research Centre (BRC-1215-20014). SJP (NIHR Career Development Fellowship, CDF-2018-11-ST2-003) is funded by the National Institute for Health Research (NIHR) for this research project. The views expressed are those of the author(s) and not necessarily those of the NIHR or the Department of Health and Social Care.

Publisher Copyright:
© 2021 by the authors. Licensee MDPI, Basel, Switzerland.

Keywords

Brain tumours
Cognitive recovery
Functional MRI
global signal
Neurosurgery

ASJC Scopus subject areas

Oncology
Cancer Research

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Access to Document

10.3390/cancers13195008Licence: Creative Commons: Attribution (CC BY)

RomeroGarciaR2021BOLDFinal published version, 4.58 MBLicence: Creative Commons: Attribution (CC BY)

Cite this

@article{8d39b2013e3e408abaf7f5d7a377c12f,

title = "Bold coupling between lesioned and healthy brain is associated with glioma patients{\textquoteright} recovery",

abstract = "Predicting functional outcomes after surgery and early adjuvant treatment is difficult due to the complex, extended, interlocking brain networks that underpin cognition. The aim of this study was to test glioma functional interactions with the rest of the brain, thereby identifying the risk factors of cognitive recovery or deterioration. Seventeen patients with diffuse non-enhancing glioma (aged 22–56 years) were longitudinally MRI scanned and cognitively assessed before and after surgery and during a 12-month recovery period (55 MRI scans in total after exclusions). We initially found, and then replicated in an independent dataset, that the spatial correlation pattern between regional and global BOLD signals (also known as global signal topography) was associated with tumour occurrence. We then estimated the coupling between the BOLD signal from within the tumour and the signal extracted from different brain tissues. We observed that the normative global signal topography is reorganised in glioma patients during the recovery period. Moreover, we found that the BOLD signal within the tumour and lesioned brain was coupled with the global signal and that this coupling was associated with cognitive recovery. Nevertheless, patients did not show any apparent disruption of functional connectivity within canonical functional networks. Understanding how tumour infiltration and coupling are related to patients{\textquoteright} recovery represents a major step forward in prognostic development.",

keywords = "Brain tumours, Cognitive recovery, Functional MRI, global signal, Neurosurgery",

author = "Rafael Romero-Garcia and Hart, {Michael G.} and Bethlehem, {Richard A.I.} and Ayan Mandal and Moataz Assem and Benedicto Crespo-Facorro and Gorriz, {Juan Manuel} and Burke, {Gladstone Austin Amos} and Price, {Stephen J.} and Thomas Santarius and Yaara Erez and John Suckling",

note = "Funding Information: This research was supported by the Guarantors of Brain, Cancer Research UK Cambridge Centre, The Brain Tumour Charity and the EMERGIA Junta de Andalucia program. Y.E. is funded by a Royal Society Dorothy Hodgkin Research Fellowship (DHF130100). JMG is funded by the Ministerio de Ciencia e Innovaci{\'o}n (Espa{\~n}a)/FEDER under the RTI2018-098913-B100 project, by the Consejer{\'i}a de Econom{\'i}a, Innovaci{\'o}n, Ciencia y Empleo (Junta de Andaluc{\'i}a) and FEDER under CV20-45250, A-TIC-080-UGR18, B-TIC-586-UGR20 and P20-00525 projects. MA was funded by a Cambridge Trust—Yousef Jameel Scholarship. This research was also supported by the NIHR Cambridge Biomedical Research Centre (BRC-1215-20014). SJP (NIHR Career Development Fellowship, CDF-2018-11-ST2-003) is funded by the National Institute for Health Research (NIHR) for this research project. The views expressed are those of the author(s) and not necessarily those of the NIHR or the Department of Health and Social Care. Publisher Copyright: {\textcopyright} 2021 by the authors. Licensee MDPI, Basel, Switzerland.",

year = "2021",

month = oct,

day = "6",

doi = "10.3390/cancers13195008",

language = "English",

volume = "13",

journal = "Cancers",

issn = "2072-6694",

publisher = "MDPI",

number = "19",

}

TY - JOUR

T1 - Bold coupling between lesioned and healthy brain is associated with glioma patients’ recovery

AU - Romero-Garcia, Rafael

AU - Hart, Michael G.

AU - Bethlehem, Richard A.I.

AU - Mandal, Ayan

AU - Assem, Moataz

AU - Crespo-Facorro, Benedicto

AU - Gorriz, Juan Manuel

AU - Burke, Gladstone Austin Amos

AU - Price, Stephen J.

AU - Santarius, Thomas

AU - Erez, Yaara

AU - Suckling, John

N1 - Funding Information: This research was supported by the Guarantors of Brain, Cancer Research UK Cambridge Centre, The Brain Tumour Charity and the EMERGIA Junta de Andalucia program. Y.E. is funded by a Royal Society Dorothy Hodgkin Research Fellowship (DHF130100). JMG is funded by the Ministerio de Ciencia e Innovación (España)/FEDER under the RTI2018-098913-B100 project, by the Consejería de Economía, Innovación, Ciencia y Empleo (Junta de Andalucía) and FEDER under CV20-45250, A-TIC-080-UGR18, B-TIC-586-UGR20 and P20-00525 projects. MA was funded by a Cambridge Trust—Yousef Jameel Scholarship. This research was also supported by the NIHR Cambridge Biomedical Research Centre (BRC-1215-20014). SJP (NIHR Career Development Fellowship, CDF-2018-11-ST2-003) is funded by the National Institute for Health Research (NIHR) for this research project. The views expressed are those of the author(s) and not necessarily those of the NIHR or the Department of Health and Social Care. Publisher Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland.

PY - 2021/10/6

Y1 - 2021/10/6

N2 - Predicting functional outcomes after surgery and early adjuvant treatment is difficult due to the complex, extended, interlocking brain networks that underpin cognition. The aim of this study was to test glioma functional interactions with the rest of the brain, thereby identifying the risk factors of cognitive recovery or deterioration. Seventeen patients with diffuse non-enhancing glioma (aged 22–56 years) were longitudinally MRI scanned and cognitively assessed before and after surgery and during a 12-month recovery period (55 MRI scans in total after exclusions). We initially found, and then replicated in an independent dataset, that the spatial correlation pattern between regional and global BOLD signals (also known as global signal topography) was associated with tumour occurrence. We then estimated the coupling between the BOLD signal from within the tumour and the signal extracted from different brain tissues. We observed that the normative global signal topography is reorganised in glioma patients during the recovery period. Moreover, we found that the BOLD signal within the tumour and lesioned brain was coupled with the global signal and that this coupling was associated with cognitive recovery. Nevertheless, patients did not show any apparent disruption of functional connectivity within canonical functional networks. Understanding how tumour infiltration and coupling are related to patients’ recovery represents a major step forward in prognostic development.

AB - Predicting functional outcomes after surgery and early adjuvant treatment is difficult due to the complex, extended, interlocking brain networks that underpin cognition. The aim of this study was to test glioma functional interactions with the rest of the brain, thereby identifying the risk factors of cognitive recovery or deterioration. Seventeen patients with diffuse non-enhancing glioma (aged 22–56 years) were longitudinally MRI scanned and cognitively assessed before and after surgery and during a 12-month recovery period (55 MRI scans in total after exclusions). We initially found, and then replicated in an independent dataset, that the spatial correlation pattern between regional and global BOLD signals (also known as global signal topography) was associated with tumour occurrence. We then estimated the coupling between the BOLD signal from within the tumour and the signal extracted from different brain tissues. We observed that the normative global signal topography is reorganised in glioma patients during the recovery period. Moreover, we found that the BOLD signal within the tumour and lesioned brain was coupled with the global signal and that this coupling was associated with cognitive recovery. Nevertheless, patients did not show any apparent disruption of functional connectivity within canonical functional networks. Understanding how tumour infiltration and coupling are related to patients’ recovery represents a major step forward in prognostic development.

KW - Brain tumours

KW - Cognitive recovery

KW - Functional MRI

KW - global signal

KW - Neurosurgery

UR - http://www.scopus.com/inward/record.url?scp=85116387705&partnerID=8YFLogxK

U2 - 10.3390/cancers13195008

DO - 10.3390/cancers13195008

M3 - Article

AN - SCOPUS:85116387705

SN - 2072-6694

VL - 13

JO - Cancers

JF - Cancers

IS - 19

M1 - 5008

ER -

Bold coupling between lesioned and healthy brain is associated with glioma patients’ recovery

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

UN SDGs

Access to Document

Fingerprint

Cite this