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J Neurol Surg A Cent Eur Neurosurg 2020; 81(06): 555-564
DOI: 10.1055/s-0040-1712496
Technical Note

Impact of Navigated Task-specific fMRI on Direct Cortical Stimulation

Joao Leote 
1   Faculdade de Ciências da Universidade de Lisboa, Instituto de Biofísica e Engenharia Biomédica, Lisboa, Portugal
2   Department of Neurosurgery and Critical Care, Hospital Garcia de Orta EPE, Almada, Portugal
,
Ricardo Loução
3   Institute of Neurosciences and Medicine, INM 4, Julich, Nordrhein-Westfalen, Germany
,
Catarina Viegas
2   Department of Neurosurgery and Critical Care, Hospital Garcia de Orta EPE, Almada, Portugal
,
Martin Lauterbach
4   Department of Neuroradiology, Sociedade Portuguesa de Ressonância Magnética, Lisboa, Portugal
,
António Perez-Hick
2   Department of Neurosurgery and Critical Care, Hospital Garcia de Orta EPE, Almada, Portugal
,
Joana Monteiro
2   Department of Neurosurgery and Critical Care, Hospital Garcia de Orta EPE, Almada, Portugal
,
Rita G. Nunes
5   Department of Bioengineering and Institute for Systems and Robotics (ISR/IST), LARSyS, Universidade de Lisboa Instituto Superior Técnico Campus Alameda, Lisboa, Lisboa, Portugal
,
Hugo A. Ferreira
1   Faculdade de Ciências da Universidade de Lisboa, Instituto de Biofísica e Engenharia Biomédica, Lisboa, Portugal
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Abstract

Background and Study Aims Cortical mapping (CM) with direct cortical stimulation (DCS) in awake craniotomy is used to preserve cognitive functions such as language. Nevertheless, patient collaboration during this procedure is influenced by previous neurological symptoms and growing discomfort with DCS duration. Our study aimed to evaluate the impact of navigated task-specific functional magnetic resonance imaging (nfMRI) on the practical aspects of DCS.

Material and Methods We recruited glioma patients scheduled for awake craniotomy for prior fMRI-based CM, acquired during motor and language tasks (i.e., verb generation, semantic and syntactic decision tasks). Language data was combined to generate a probabilistic map indicating brain regions activated with more than one paradigm. Presurgical neurophysiological language tests (i.e., verb generation, picture naming, and semantic tasks) were also performed. We considered for subsequent study only the patients with a minimum rate of correct responses of 50% in all tests. These patients were then randomized to perform intraoperative language CM either using the multimodal approach (mCM), using nfMRI and DCS combined, or electrical CM (eCM), with DCS alone. DCS was done while the patient performed picture naming and nonverbal semantic decision tasks. Methodological features such as DCS duration, number of stimuli, total delivered stimulus duration per task, and frequency of seizures were analyzed and compared between groups. The correspondence between positive responses obtained with DCS and nfMRI was also evaluated.

Results Twenty-one surgeries were included, thirteen of which using mCM (i.e., test group). Patients with lower presurgical neuropsychological performance (correct response rate between 50 and 80% in language tests) showed a decreased DCS duration in comparison with the control group. None of the compared methodological features showed differences between groups. Correspondence between DCS and nfMRI was 100/84% in the identification of the precentral gyrus for motor function/opercular frontal inferior gyrus for language function, respectively.

Conclusion Navigated fMRI data did not influence DCS in practice. Presurgical language disturbances limited the applicability of DCS mapping in awake surgery.

Keywords

glioma - awake surgery - navigated functional magnetic resonance imaging - direct cortical stimulation


Publication History

Received: 31 July 2019

Accepted: 02 December 2019

Article published online:
01 July 2020

© 2020. Thieme. All rights reserved.

Georg Thieme Verlag KG
Stuttgart · New York

 

  • References

  • 1 Hickok G, Poeppel D. The cortical organization of speech processing. Nat Rev Neurosci 2007; 8 (05) 393-402
    Google Scholar
  • 2 Eyüpoglu IY, Buchfelder M, Savaskan NE. Surgical resection of malignant gliomas-role in optimizing patient outcome. Nat Rev Neurol 2013; 9 (03) 141-151
    CrossrefPubMedGoogle Scholar
  • 3 Tuominen J, Yrjänä S, Ukkonen A, Koivukangas J. Awake craniotomy may further improve neurological outcome of intraoperative MRI-guided brain tumor surgery. Acta Neurochir (Wien) 2013; 155 (10) 1805-1812
    CrossrefPubMedGoogle Scholar
  • 4 Beez T, Boge K, Wager M. et al; European Low Grade Glioma Network. Tolerance of awake surgery for glioma: a prospective European Low Grade Glioma Network multicenter study. Acta Neurochir (Wien) 2013; 155 (07) 1301-1308
    CrossrefPubMedGoogle Scholar
  • 5 Dineen J, Maus DC, Muzyka I. et al. Factors that modify the risk of intraoperative seizures triggered by electrical stimulation during supratentorial functional mapping. Clin Neurophysiol 2019; 130 (06) 1058-1065
    CrossrefPubMedGoogle Scholar
  • 6 Milian M, Tatagiba M, Feigl GC. Patient response to awake craniotomy - a summary overview. Acta Neurochir (Wien) 2014; 156 (06) 1063-1070
    CrossrefPubMedGoogle Scholar
  • 7 Vakamudi K, Posse S, Jung R, Cushnyr B, Chohan MO. Real-time presurgical resting-state fMRI in patients with brain tumors: Quality control and comparison with task-fMRI and intraoperative mapping. Hum Brain Mapp 2019; 6 DOI: 10.1002/hbm.24840.
    CrossrefPubMedGoogle Scholar
  • 8 Peck KK, Bradbury M, Petrovich N. et al. Presurgical evaluation of language using functional magnetic resonance imaging in brain tumor patients with previous surgery. Neurosurgery 2009; 64 (04) 644-652 , discussion 652–653
    CrossrefPubMedGoogle Scholar
  • 9 Benjamin CF, Walshaw PD, Hale K. et al. Presurgical language fMRI: Mapping of six critical regions. Hum Brain Mapp 2017; 38 (08) 4239-4255
    CrossrefPubMedGoogle Scholar
  • 10 Ille S, Sollmann N, Hauck T. et al. Impairment of preoperative language mapping by lesion location: a functional magnetic resonance imaging, navigated transcranial magnetic stimulation, and direct cortical stimulation study. J Neurosurg 2015; 123 (02) 314-324
    CrossrefPubMedGoogle Scholar
  • 11 Jenkinson MD, Barone DG, Bryant A. et al. Intraoperative imaging technology to maximise extent of resection for glioma. Cochrane Database Syst Rev 2018; 1: CD012788
    PubMedGoogle Scholar
  • 12 Gaillard WD, Balsamo L, Xu B. et al. fMRI language task panel improves determination of language dominance. Neurology 2004; 63 (08) 1403-1408
    CrossrefPubMedGoogle Scholar
  • 13 Kim S, Jin T, Fukuda M. Spatial Resolution of fMRI Techniques. In: Ulmer S, Jansen O. (eds) fMRI. Springer; Berlin, Heidelberg: 2010: 15-21
    CrossrefGoogle Scholar
  • 14 Holodny AI, Schulder M, Liu WC, Wolko J, Maldjian JA, Kalnin AJ. The effect of brain tumors on BOLD functional MR imaging activation in the adjacent motor cortex: implications for image-guided neurosurgery. AJNR Am J Neuroradiol 2000; 21 (08) 1415-1422
    PubMedGoogle Scholar
  • 15 Wang L, Chen D, Olson J, Ali S, Fan T, Mao H. Re-examine tumor-induced alterations in hemodynamic responses of BOLD fMRI: implications in presurgical brain mapping. Acta Radiol 2012; 53 (07) 802-811
    CrossrefPubMedGoogle Scholar
  • 16 Castro S, Gomes I, Caló S. PALPA-P – Provas de Avaliação da Linguagem e da Afasia em. Português, Lisboa: CEGOC; 2007
    Google Scholar
  • 17 Soffietti R, Baumert BG, Bello L. et al; European Federation of Neurological Societies. Guidelines on management of low-grade gliomas: report of an EFNS-EANO Task Force. Eur J Neurol 2010; 17 (09) 1124-1133
    CrossrefPubMedGoogle Scholar
  • 18 Weller M, van den Bent M, Hopkins K. et al; European Association for Neuro-Oncology (EANO) Task Force on Malignant Glioma. EANO guideline for the diagnosis and treatment of anaplastic gliomas and glioblastoma. Lancet Oncol 2014; 15 (09) e395-e403 Erratum in: Lancet Oncol. 2014; 15: e587
    CrossrefPubMedGoogle Scholar
  • 19 Goebel R, Esposito F, Formisano E. Analysis of functional image analysis contest (FIAC) data with brainvoyager QX: From single-subject to cortically aligned group general linear model analysis and self-organizing group independent component analysis. Hum Brain Mapp 2006; 27 (05) 392-401
    CrossrefPubMedGoogle Scholar
  • 20 Hund-Georgiadis M, Lex U, von Cramon DY. Language dominance assessment by means of fMRI: contributions from task design, performance, and stimulus modality. J Magn Reson Imaging 2001; 13 (05) 668-675
    CrossrefPubMedGoogle Scholar
  • 21 Schulte-Tamburen AM, Scheier J, Briegel J, Schwender D, Peter K. Comparison of five sedation scoring systems by means of auditory evoked potentials. Intensive Care Med 1999; 25 (04) 377-382
    CrossrefPubMedGoogle Scholar
  • 22 Corina DP, Gibson EK, Martin R, Poliakov A, Brinkley J, Ojemann GA. Dissociation of action and object naming: evidence from cortical stimulation mapping. Hum Brain Mapp 2005; 24 (01) 1-10
    CrossrefPubMedGoogle Scholar
  • 23 Duffau H, Capelle L, Denvil D. et al. Usefulness of intraoperative electrical subcortical mapping during surgery for low-grade gliomas located within eloquent brain regions: functional results in a consecutive series of 103 patients. J Neurosurg 2003; 98 (04) 764-778
    CrossrefPubMedGoogle Scholar
  • 24 Weng HH, Noll KR, Johnson JM. et al. Accuracy of Presurgical Functional MR Imaging for Language Mapping of Brain Tumors: A Systematic Review and Meta-Analysis. Radiology 2018; 286 (02) 512-523
    CrossrefPubMedGoogle Scholar
  • 25 Sabsevitz DS, Swanson SJ, Hammeke TA. et al. Use of preoperative functional neuroimaging to predict language deficits from epilepsy surgery. Neurology 2003; 60 (11) 1788-1792
    CrossrefPubMedGoogle Scholar
  • 26 Gauthier CJ, Fan AP. BOLD signal physiology: Models and applications. Neuroimage 2019; 187: 116-127
    CrossrefPubMedGoogle Scholar
  • 27 Morrison MA, Tam F, Garavaglia MM. et al. A novel tablet computer platform for advanced language mapping during awake craniotomy procedures. J Neurosurg 2016; 124 (04) 938-944
    CrossrefPubMedGoogle Scholar
  • 28 Binder J. Use of fMRI Language Lateralization for Quantitative Prediction of Naming and Verbal Memory Outcome in Left Temporal Lobe Epilepsy Surgery. In: Ulmer S, Jansen O. , eds. fMRI. Berlin, Heidelberg: Springer; 2013: 77-93
    CrossrefGoogle Scholar
  • 29 Mehdorn H, Goebel S, Nabavi A. Direct Cortical Stimulation and fMRI. In: Ulmer S, Jansen O. , eds. fMRI – Basics and Clinical Applications. Berlin: Springer; 2013: 169-175
    Google Scholar
  • 30 Hall WA, Kim P, Truwit CL. Functional magnetic resonance imaging-guided brain tumor resection. Top Magn Reson Imaging 2009; 19 (04) 205-212
    CrossrefPubMedGoogle Scholar
  • 31 De Witte E, Satoer D, Robert E. et al. The Dutch Linguistic Intraoperative Protocol: a valid linguistic approach to awake brain surgery. Brain Lang 2015; 140: 35-48
    CrossrefPubMedGoogle Scholar
  • 32 De Witte E, Mariën P. The neurolinguistic approach to awake surgery reviewed. Clin Neurol Neurosurg 2013; 115 (02) 127-145
    CrossrefPubMedGoogle Scholar
  • 33 Roux FE, Ibarrola D, Tremoulet M. et al. Methodological and technical issues for integrating functional magnetic resonance imaging data in a neuronavigational system. Neurosurgery 2001; 49 (05) 1145-1156 , discussion 1156–1157
    CrossrefPubMedGoogle Scholar
  • 34 Strappini F, Gilboa E, Pitzalis S. et al. Adaptive smoothing based on Gaussian processes regression increases the sensitivity and specificity of fMRI data. Hum Brain Mapp 2017; 38 (03) 1438-1459
    CrossrefPubMedGoogle Scholar
  • 35 Stieglitz LH, Fichtner J, Andres R. et al. The silent loss of neuronavigation accuracy: a systematic retrospective analysis of factors influencing the mismatch of frameless stereotactic systems in cranial neurosurgery. Neurosurgery 2013; 72 (05) 796-807
    CrossrefPubMedGoogle Scholar
  • 36 Jen ML, Hassan I, Hou P. et al. Comparison of functional localization accuracy with different co-registration strategies in presurgical fMRI for brain tumor patients. Med Phys 2018; 45 (07) 3223-3228
    CrossrefPubMedGoogle Scholar
  • 37 Szelényi A, Bello L, Duffau H. et al; Workgroup for Intraoperative Management in Low-Grade Glioma Surgery within the European Low-Grade Glioma Network. Intraoperative electrical stimulation in awake craniotomy: methodological aspects of current practice. Neurosurg Focus 2010; 28 (02) E7
    CrossrefPubMedGoogle Scholar
  • 38 Nossek E, Matot I, Shahar T. et al. Failed awake craniotomy: a retrospective analysis in 424 patients undergoing craniotomy for brain tumor. J Neurosurg 2013; 118 (02) 243-249
    CrossrefPubMedGoogle Scholar
  • 39 Chang EF, Breshears JD, Raygor KP, Lau D, Molinaro AM, Berger MS. Stereotactic probability and variability of speech arrest and anomia sites during stimulation mapping of the language dominant hemisphere. J Neurosurg 2017; 126 (01) 114-121
    CrossrefPubMedGoogle Scholar