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Article

BOLD Coupling between Lesioned and Healthy Brain Is Associated with Glioma Patients’ Recovery

1
Department of Psychiatry, University of Cambridge, Cambridge CB2 0SZ, UK
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Department of Medical Physiology and Biophysics, Instituto de Biomedicina de Sevilla (IBiS), HUVR/CSIC/Universidad de Sevilla, 41013 Sevilla, Spain
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MRC Cognition and Brain Sciences Unit, University of Cambridge, Cambridge CB2 7EF, UK
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Department of Psychiatry, Instituto de Investigación Sanitaria de Sevilla, IBiS, Hospital Universitario Virgen del Rocio, CIBERSAM, 41013 Sevilla, Spain
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Department of Signal Theory, Networking and Communications, Universidad de Granada, 18071 Granada, Spain
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Department of Paediatric Haematology, Oncology and Palliative Care, Addenbrooke’s Hospital, Cambridge CB2 0QQ, UK
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Academic Neurosurgery Division, Department of Clinical Neurosciences, University of Cambridge, Cambridge CB2 0QQ, UK
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Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge CB2 0SZ, UK
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Faculty of Engineering, Bar-Ilan University, Ramat Gan 5290002, Israel
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Behavioural and Clinical Neuroscience Institute, University of Cambridge, Cambridge CB2 0SZ, UK
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Cambridge and Peterborough NHS Foundation Trust, Cambridge CB21 5EF, UK
*
Author to whom correspondence should be addressed.
Academic Editors: Bernhard Meyer, Sandro Krieg, Jens Gempt and Shinji Kawabata
Cancers 2021, 13(19), 5008; https://doi.org/10.3390/cancers13195008
Received: 21 July 2021 / Revised: 30 September 2021 / Accepted: 1 October 2021 / Published: 6 October 2021
(This article belongs to the Special Issue Perioperative Imaging and Mapping Methods in Glioma Patients)
Glioma, a type of brain tumour, affects not only the function of immediately adjacent brain tissue but also that in more distant areas, potentially impacting cognitive function after its surgical removal. Here, 17 patients with glioma had brain scans and tests of cognitive function during treatment and recovery. We investigated the effects of glioma on the brain, and what happens during recovery, using the brain’s “global signal” detected with magnetic resonance imaging (MRI). We found that the signal from gliomas was synchronised with the global signal in all patients and that this synchronisation was associated with the recovery of cognition after surgery. Specifically, patients with a greater reduction in glioma–global signal synchronisation following surgery were more likely to have a larger number of newly acquired cognitive difficulties. Together, these results suggest that the interaction between gliomas and the brain can predict how patients recover their cognitive abilities, which is important for their quality of life.
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. View Full-Text
Keywords: global signal; brain tumours; functional MRI; neurosurgery; cognitive recovery global signal; brain tumours; functional MRI; neurosurgery; cognitive recovery
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MDPI and ACS Style

Romero-Garcia, R.; Hart, M.G.; Bethlehem, R.A.I.; Mandal, A.; Assem, M.; Crespo-Facorro, B.; Gorriz, J.M.; Burke, G.A.A.; Price, S.J.; Santarius, T.; Erez, Y.; Suckling, J. BOLD Coupling between Lesioned and Healthy Brain Is Associated with Glioma Patients’ Recovery. Cancers 2021, 13, 5008. https://doi.org/10.3390/cancers13195008

AMA Style

Romero-Garcia R, Hart MG, Bethlehem RAI, Mandal A, Assem M, Crespo-Facorro B, Gorriz JM, Burke GAA, Price SJ, Santarius T, Erez Y, Suckling J. BOLD Coupling between Lesioned and Healthy Brain Is Associated with Glioma Patients’ Recovery. Cancers. 2021; 13(19):5008. https://doi.org/10.3390/cancers13195008

Chicago/Turabian Style

Romero-Garcia, Rafael, Michael G. Hart, Richard A. I. Bethlehem, Ayan Mandal, Moataz Assem, Benedicto Crespo-Facorro, Juan Manuel Gorriz, G. A. Amos Burke, Stephen J. Price, Thomas Santarius, Yaara Erez, and John Suckling. 2021. "BOLD Coupling between Lesioned and Healthy Brain Is Associated with Glioma Patients’ Recovery" Cancers 13, no. 19: 5008. https://doi.org/10.3390/cancers13195008

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