Resting-state functional MRI in an intraoperative MRI setting: proof of feasibility and correlation to clinical outcome of patients

Constantin Roder Departments of Neurosurgery,

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Edyta Charyasz-Leks Neuroradiology, and
Department of Biomedical Magnetic Resonance, University of Tübingen, and Eberhard Karls University, Tübingen, Germany; and

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Martin Breitkopf Departments of Neurosurgery,

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Karlheinz Decker Anaesthesiology, Eberhard Karls University;

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Ulrike Ernemann Neuroradiology, and

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Uwe Klose Neuroradiology, and

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Marcos Tatagiba Departments of Neurosurgery,

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Sotirios Bisdas Neuroradiology, and
Lysholm Department of Neuroradiology, National Hospital for Neurology and Neurosurgery, University College London Hospitals, London, United Kingdom

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OBJECTIVE

The authors' aim in this paper is to prove the feasibility of resting-state (RS) functional MRI (fMRI) in an intraoperative setting (iRS-fMRI) and to correlate findings with the clinical condition of patients pre- and postoperatively.

METHODS

Twelve patients underwent intraoperative MRI-guided resection of lesions in or directly adjacent to the central region and/or pyramidal tract. Intraoperative RS (iRS)–fMRI was performed pre- and intraoperatively and was correlated with patients' postoperative clinical condition, as well as with intraoperative monitoring results. Independent component analysis (ICA) was used to postprocess the RS-fMRI data concerning the sensorimotor networks, and the mean z-scores were statistically analyzed.

RESULTS

iRS-fMRI in anesthetized patients proved to be feasible and analysis revealed no significant differences in preoperative z-scores between the sensorimotor areas ipsi- and contralateral to the tumor. A significant decrease in z-score (p < 0.01) was seen in patients with new neurological deficits postoperatively. The intraoperative z-score in the hemisphere ipsilateral to the tumor had a significant negative correlation with the degree of paresis immediately after the operation (r = −0.67, p < 0.001) and on the day of discharge from the hospital (r = −0.65, p < 0.001). Receiver operating characteristic curve analysis demonstrated moderate prognostic value of the intraoperative z-score (area under the curve 0.84) for the paresis score at patient discharge.

CONCLUSIONS

The use of iRS-fMRI with ICA-based postprocessing and functional activity mapping is feasible and the results may correlate with clinical parameters, demonstrating a significant negative correlation between the intensity of the iRS-fMRI signal and the postoperative neurological changes.

ABBREVIATIONS

fMRI = functional MRI; ICA = independent component analysis; iMRI = intraoperative MRI; IOM = intraoperative monitoring; iRS-fMRI = intraoperative resting-state fMRI; MEP = motor evoked potential; ROC = receiver operating characteristic; RS = resting state; RSN = RS network; SMA = supplementary motor area; SMN = sensorimotor network; SSEP = somatosensory evoked potential.
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  • 1

    Allen EA, , Erhardt EB, , Damaraju E, , Gruner W, , Segall JM, & Silva RF, et al.: A baseline for the multivariate comparison of resting-state networks. Front Syst Neurosci 5:2, 2011

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Bell AJ, & Sejnowski TJ: An information-maximization approach to blind separation and blind deconvolution. Neural Comput 7:11291159, 1995

  • 3

    Boly M, , Tshibanda L, , Vanhaudenhuyse A, , Noirhomme Q, , Schnakers C, & Ledoux D, et al.: Functional connectivity in the default network during resting state is preserved in a vegetative but not in a brain dead patient. Hum Brain Mapp 30:23932400, 2009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Boveroux P, , Vanhaudenhuyse A, , Bruno MA, , Noirhomme Q, , Lauwick S, & Luxen A, et al.: Breakdown of within- and between-network resting state functional magnetic resonance imaging connectivity during propofol-induced loss of consciousness. Anesthesiology 113:10381053, 2010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Chen X, , Xu BN, , Meng X, , Zhang J, , Yu X, & Zhou D: Dualroom 1.5-T intraoperative magnetic resonance imaging suite with a movable magnet: implementation and preliminary experience. Neurosurg Rev 35:95110, 2012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Cole DM, , Smith SM, & Beckmann CF: Advances and pitfalls in the analysis and interpretation of resting-state FMRI data. Front Syst Neurosci 4:8, 2010

  • 7

    Kokkonen SM, , Nikkinen J, , Remes J, , Kantola J, , Starck T, & Haapea M, et al.: Preoperative localization of the sensorimotor area using independent component analysis of resting-state fMRI. Magn Reson Imaging 27:733740, 2009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Kollndorfer K, , Fischmeister FP, , Kasprian G, , Prayer D, & Schöpf V: A systematic investigation of the invariance of resting-state network patterns: is resting-state fMRI ready for pre-surgical planning?. Front Hum Neurosci 7:95, 2013

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Krieg SM, , Shiban E, , Droese D, , Gempt J, , Buchmann N, & Pape H, et al.: Predictive value and safety of intraoperative neurophysiological monitoring with motor evoked potentials in glioma surgery. Neurosurgery 70:10601071, 2012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Kubben PL, , ter Meulen KJ, , Schijns OEMG, , ter Laak-Poort MP, , van Overbeeke JJ, & van Santbrink H: Intraoperative MRI-guided resection of glioblastoma multiforme: a systematic review. Lancet Oncol 12:10621070, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Kuhnt D, , Bauer MHA, , Becker A, , Merhof D, , Zolal A, & Richter M, et al.: Intraoperative visualization of fiber tracking based reconstruction of language pathways in glioma surgery. Neurosurgery 70:911920, 2012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Lang S, , Duncan N, & Northoff G: Resting-state functional magnetic resonance imaging: review of neurosurgical applications. Neurosurgery 74:453465, 2014

  • 13

    Larson-Prior LJ, , Power JD, , Vincent JL, , Nolan TS, , Coalson RS, & Zempel J, et al.: Modulation of the brain's functional network architecture in the transition from wake to sleep. Prog Brain Res 193:277294, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Larson-Prior LJ, , Zempel JM, , Nolan TS, , Prior FW, , Snyder AZ, & Raichle ME: Cortical network functional connectivity in the descent to sleep. Proc Natl Acad Sci U S A 106:44894494, 2009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Lee MH, , Smyser CD, & Shimony JS: Resting-state fMRI: a review of methods and clinical applications. AJNR Am J Neuroradiol 34:18661872, 2013

  • 16

    Ma L, , Wang B, , Chen X, & Xiong J: Detecting functional connectivity in the resting brain: a comparison between ICA and CCA. Magn Reson Imaging 25:4756, 2007

  • 17

    Neuloh G, , Pechstein U, , Cedzich C, & Schramm J: Motor evoked potential monitoring with supratentorial surgery. Neurosurgery 54:10611072, 2004

  • 18

    Nimsky C: Intraoperative acquisition of fMRI and DTI. Neurosurg Clin N Am 22:269277, ix, 2011

  • 19

    Quigley M, , Cordes D, , Wendt G, , Turski P, , Moritz C, & Haughton V, et al.: Effect of focal and nonfocal cerebral lesions on functional connectivity studied with MR imaging. AJNR Am J Neuroradiol 22:294300, 2001

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Roder C, , Bender B, , Ritz R, , Honegger J, , Feigl G, & Naegele T, et al.: Intraoperative visualization of residual tumor: the role of perfusion-weighted imaging in a high-field intraoperative magnetic resonance scanner. Neurosurgery 72:2 Suppl Operative ons151ons158, 2013

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Roder C, , Bisdas S, , Ebner FH, , Honegger J, , Naegele T, & Ernemann U, et al.: Maximizing the extent of resection and survival benefit of patients in glioblastoma surgery: high-field iMRI versus conventional and 5-ALA-assisted surgery. Eur J Surg Oncol 40:297304, 2014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Roder C, , Skardelly M, , Ramina KF, , Beschorner R, , Honneger J, & Nägele T, et al.: Spectroscopy imaging in intraoperative MR suite: tissue characterization and optimization of tumor resection. Int J CARS 9:551559, 2014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Roessler K, , Donat M, , Lanzenberger R, , Novak K, , Geissler A, & Gartus A, et al.: Evaluation of preoperative high magnetic field motor functional MRI (3 Tesla) in glioma patients by navigated electrocortical stimulation and postoperative outcome. J Neurol Neurosurg Psychiatry 76:11521157, 2005

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Seidel K, , Beck J, , Stieglitz L, , Schucht P, & Raabe A: The warning-sign hierarchy between quantitative subcortical motor mapping and continuous motor evoked potential monitoring during resection of supratentorial brain tumors. J Neurosurg 118:287296, 2013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Soddu A, , Vanhaudenhuyse A, , Bahri MA, , Bruno MA, , Boly M, & Demertzi A, et al.: Identifying the default-mode component in spatial IC analyses of patients with disorders of consciousness. Hum Brain Mapp 33:778796, 2012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Stufflebeam SM, , Liu H, , Sepulcre J, , Tanaka N, , Buckner RL, & Madsen JR: Localization of focal epileptic discharges using functional connectivity magnetic resonance imaging. J Neurosurg 114:16931697, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    van den Heuvel MP, & Hulshoff Pol HE: Exploring the brain network: a review on resting-state fMRI functional connectivity. Eur Neuropsychopharmacol 20:519534, 2010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Zhang D, , Johnston JM, , Fox MD, , Leuthardt EC, , Grubb RL, & Chicoine MR, et al.: Preoperative sensorimotor mapping in brain tumor patients using spontaneous fluctuations in neuronal activity imaged with functional magnetic resonance imaging: initial experience. Neurosurgery 65:6 Suppl 226236, 2009

    • PubMed
    • Search Google Scholar
    • Export Citation

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