Literature DB >> 32244221

The impact of high functional connectivity network hub resection on language task performance in adult low- and high-grade glioma.

Anthony T Lee1, Claire Faltermeier1, Ramin A Morshed1, Jacob S Young1, Sofia Kakaizada1, Claudia Valdivia1, Anne M Findlay2, Phiroz E Tarapore1, Srikantan S Nagarajan2, Shawn L Hervey-Jumper1, Mitchel S Berger1.   

Abstract

OBJECTIVE: Gliomas are intrinsic brain tumors with the hallmark of diffuse white matter infiltration, resulting in short- and long-range network dysfunction. Preoperative magnetoencephalography (MEG) can assist in maximizing the extent of resection while minimizing morbidity. While MEG has been validated in motor mapping, its role in speech mapping remains less well studied. The authors assessed how the resection of intraoperative electrical stimulation (IES)-negative, high functional connectivity (HFC) network sites, as identified by MEG, impacts language performance.
METHODS: Resting-state, whole-brain MEG recordings were obtained from 26 patients who underwent perioperative language evaluation and glioma resection that was guided by awake language and IES mapping. The functional connectivity of an individual voxel was determined by the imaginary coherence between the index voxel and the rest of the brain, referenced to its contralesional pair. The percentage of resected HFC voxels was correlated with postoperative language outcomes in tasks of increasing complexity: text reading, 4-syllable repetition, picture naming, syntax (SYN), and auditory stimulus naming (AN).
RESULTS: Overall, 70% of patients (14/20) in whom any HFC tissue was resected developed an early postoperative language deficit (mean 2.3 days, range 1-8 days), compared to 33% of patients (2/6) in whom no HFC tissue was resected (p = 0.16). When bifurcated by the amount of HFC tissue that was resected, 100% of patients (3/3) with an HFC resection > 25% displayed deficits in AN, compared to 30% of patients (6/20) with an HFC resection < 25% (p = 0.04). Furthermore, there was a linear correlation between the severity of AN and SYN decline with percentage of HFC sites resected (p = 0.02 and p = 0.04, respectively). By 2.2 months postoperatively (range 1-6 months), the correlation between HFC resection and both AN and SYN decline had resolved (p = 0.94 and p = 1.00, respectively) in all patients (9/9) except two who experienced early postoperative tumor progression or stroke involving inferior frontooccipital fasciculus.
CONCLUSIONS: Imaginary coherence measures of functional connectivity using MEG are able to identify HFC network sites within and around low- and high-grade gliomas. Removal of IES-negative HFC sites results in early transient postoperative decline in AN and SYN, which resolved by 3 months in all patients without stroke or early tumor progression. Measures of functional connectivity may therefore be a useful means of counseling patients about postoperative risk and assist with preoperative surgical planning.

Entities:  

Keywords:  functional connectivity; glioblastoma; high-grade glioma; language; low-grade glioma; magnetoencephalography; oncology; speech

Mesh:

Year:  2020        PMID: 32244221      PMCID: PMC8011942          DOI: 10.3171/2020.1.JNS192267

Source DB:  PubMed          Journal:  J Neurosurg        ISSN: 0022-3085            Impact factor:   5.115


  45 in total

1.  Functional recovery after surgical resection of low grade gliomas in eloquent brain: hypothesis of brain compensation.

Authors:  H Duffau; L Capelle; D Denvil; N Sichez; P Gatignol; M Lopes; M-C Mitchell; J-P Sichez; R Van Effenterre
Journal:  J Neurol Neurosurg Psychiatry       Date:  2003-07       Impact factor: 10.154

2.  Synchronized brain activity and neurocognitive function in patients with low-grade glioma: a magnetoencephalography study.

Authors:  Ingeborg Bosma; Linda Douw; Fabrice Bartolomei; Jan J Heimans; Bob W van Dijk; Tjeerd J Postma; Cornelis J Stam; Jaap C Reijneveld; Martin Klein
Journal:  Neuro Oncol       Date:  2008-07-23       Impact factor: 12.300

Review 3.  Contemporary model of language organization: an overview for neurosurgeons.

Authors:  Edward F Chang; Kunal P Raygor; Mitchel S Berger
Journal:  J Neurosurg       Date:  2014-11-28       Impact factor: 5.115

4.  How do brain tumors alter functional connectivity? A magnetoencephalography study.

Authors:  Fabrice Bartolomei; Ingeborg Bosma; Martin Klein; Johannes C Baayen; Jaap C Reijneveld; Tjeerd J Postma; Jan J Heimans; Bob W van Dijk; Jan C de Munck; Arent de Jongh; Keith S Cover; Cornelis J Stam
Journal:  Ann Neurol       Date:  2006-01       Impact factor: 10.422

Review 5.  New concepts in surgery of WHO grade II gliomas: functional brain mapping, connectionism and plasticity--a review.

Authors:  Hugues Duffau
Journal:  J Neurooncol       Date:  2006-04-11       Impact factor: 4.130

6.  Five-dimensional neuroimaging: localization of the time-frequency dynamics of cortical activity.

Authors:  Sarang S Dalal; Adrian G Guggisberg; Erik Edwards; Kensuke Sekihara; Anne M Findlay; Ryan T Canolty; Mitchel S Berger; Robert T Knight; Nicholas M Barbaro; Heidi E Kirsch; Srikantan S Nagarajan
Journal:  Neuroimage       Date:  2008-01-31       Impact factor: 6.556

7.  Functional outcome after language mapping for glioma resection.

Authors:  Nader Sanai; Zaman Mirzadeh; Mitchel S Berger
Journal:  N Engl J Med       Date:  2008-01-03       Impact factor: 91.245

8.  Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients.

Authors:  G Ojemann; J Ojemann; E Lettich; M Berger
Journal:  J Neurosurg       Date:  1989-09       Impact factor: 5.115

9.  Cognitive Impairments in Schizophrenia as Assessed Through Activation and Connectivity Measures of Magnetoencephalography (MEG) Data.

Authors:  Leighton B N Hinkley; Julia P Owen; Melissa Fisher; Anne M Findlay; Sophia Vinogradov; Srikantan S Nagarajan
Journal:  Front Hum Neurosci       Date:  2010-11-11       Impact factor: 3.169

10.  The influence of low-grade glioma on resting state oscillatory brain activity: a magnetoencephalography study.

Authors:  I Bosma; C J Stam; L Douw; F Bartolomei; J J Heimans; B W van Dijk; T J Postma; M Klein; J C Reijneveld
Journal:  J Neurooncol       Date:  2008-02-08       Impact factor: 4.130

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  7 in total

1.  Functional alterations in cortical processing of speech in glioma-infiltrated cortex.

Authors:  Alexander A Aabedi; Benjamin Lipkin; Jasleen Kaur; Sofia Kakaizada; Claudia Valdivia; Sheantel Reihl; Jacob S Young; Anthony T Lee; Saritha Krishna; Mitchel S Berger; Edward F Chang; David Brang; Shawn L Hervey-Jumper
Journal:  Proc Natl Acad Sci U S A       Date:  2021-11-16       Impact factor: 11.205

2.  Dynamical Mechanism Underlying Scale-Free Network Reorganization in Low Acetylcholine States Corresponding to Slow Wave Sleep.

Authors:  Paulina Czarnecki; Jack Lin; Sara J Aton; Michal Zochowski
Journal:  Front Netw Physiol       Date:  2021-10-25

3.  Convergence of heteromodal lexical retrieval in the lateral prefrontal cortex.

Authors:  David Brang; Shawn L Hervey-Jumper; Alexander A Aabedi; Sofia Kakaizada; Jacob S Young; Jasleen Kaur; Olivia Wiese; Claudia Valdivia; Saritha Krishna; Christina Weyer-Jamora; Mitchel S Berger; Daniel H Weissman
Journal:  Sci Rep       Date:  2021-03-18       Impact factor: 4.379

Review 4.  Advanced Imaging Techniques for Newly Diagnosed and Recurrent Gliomas.

Authors:  Luis R Carrete; Jacob S Young; Soonmee Cha
Journal:  Front Neurosci       Date:  2022-02-23       Impact factor: 4.677

Review 5.  Involvement of White Matter Language Tracts in Glioma: Clinical Implications, Operative Management, and Functional Recovery After Injury.

Authors:  Alexander A Aabedi; Jacob S Young; Edward F Chang; Mitchel S Berger; Shawn L Hervey-Jumper
Journal:  Front Neurosci       Date:  2022-07-11       Impact factor: 5.152

6.  Influences on cognitive outcomes in adult patients with gliomas: A systematic review.

Authors:  Matthew A Kirkman; Benjamin H M Hunn; Michael S C Thomas; Andrew K Tolmie
Journal:  Front Oncol       Date:  2022-08-05       Impact factor: 5.738

Review 7.  Functional Mapping before and after Low-Grade Glioma Surgery: A New Way to Decipher Various Spatiotemporal Patterns of Individual Neuroplastic Potential in Brain Tumor Patients.

Authors:  Hugues Duffau
Journal:  Cancers (Basel)       Date:  2020-09-13       Impact factor: 6.639

  7 in total

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