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Preoperative and intraoperative brain mapping for the resection of eloquent-area tumors. A prospective analysis of methodology, correlation, and usefulness based on clinical outcomes

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Abstract

Background

Localization of brain function is a fundamental requisite for the resection of eloquent-area brain tumors. Preoperative functional neuroimaging and diffusion tensor imaging can display cortical functional organization and subcortical anatomy of major white matter bundles. Direct cortical and subcortical stimulation is widely used in routine practice, however, because of its ability to reveal tissue function in eloquent regions. The role and integration of these techniques is still a matter of debate. The objective of this study was to assess surgical and functional neurological outputs of awake surgery and intraoperative cortical and subcortical electrical stimulation (CSES) and to use CSES to examine the reliability of preoperative functional magnetic resonance (fMRI) and diffusion tensor imaging fiber tracking (DTI-FT) for surgical planning.

Patients and methods

We prospectively studied 27 patients with eloquent-area tumors who were selected to undergo awake surgery and direct brain mapping. All subjects underwent preoperative sensorimotor and language fMRI and DTI tractography of major white matter bundles. Intra- and postoperative complications, stimulation effects, extent of resection, and neurological outcome were determined. We topographically correlated intraoperatively identified sites (cortical and subcortical) with areas of fMRI activation and DTI tractography.

Results

Total plus subtotal resection reached 88.8%. Twenty-one patients (77.7%) suffered transient postoperative worsening, but at 6 months follow-up only three (11.1%) patients had persistent neurological impairment. Sensorimotor cortex direct mapping correlated 92.3% with fMRI activation, while direct mapping of language cortex correlated 42.8%. DTI fiber tracking underestimated the presence of functional fibers surrounding or inside the tumor.

Conclusion

Preoperative brain mapping is useful when planning awake surgery to estimate the relationship between the tumor and functional brain regions. However, these techniques cannot directly lead the surgeon during resection. Intraoperative brain mapping is necessary for safe and maximal resection and to guarantee a satisfying neurological outcome. This multimodal approach is more aggressive, leads to better outcomes, and should be used routinely for resection of lesions in eloquent brain regions.

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Abbreviations

fMRI:

Functional Magnetic Resonance

DTI-FT:

Diffusion Tensor Imaging Fiber Tracking

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Authors and Affiliations

  1. Division of Neurosurgery, Civil Hospital, via Venezia 16, 15100, Alessandria, Italy

    Giannantonio Spena & Pietro Versari

  2. Anesthesiology and Intensive Care Unit Department, Civil Hospital, Alessandria, Italy

    Antonella Nava & Fabrizio Cassini

  3. Division of Neurology and Neuropsychology, Civil Hospital, Alessandria, Italy

    Antonio Pepoli, Marcella Bruno & Laura Barletta

  4. CCS fMRI, Koelliker Hospital and Department of Psychology, University of Turin, Turin, Italy

    Federico D’Agata, Franco Cauda, Katiuscia Sacco & Sergio Duca

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  1. Giannantonio Spena
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  2. Antonella Nava
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  3. Fabrizio Cassini
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  4. Antonio Pepoli
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Correspondence to Giannantonio Spena.

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Comment

The authors have prospectively studied 27 patients who underwent surgery for a lesion located within eloquent brain areas. Functional mapping was performed by combining preoperative fMRI and DTI as well as intrasurgical electrostimulation in awake patients. The authors conclude that, although preoperative functional neuroimaging is useful, intraoperative mapping is still necessary for safe and maximal resection of lesions in eloquent areas.

This is a very interesting article, for several reasons (1) it is a prospective series (even if the number of patients is small); (2) correlations have been made between fMRI and cortical stimulation as well as between DTI and subcortical stimulation, concerning both sensorimotor and language functions: they demonstrate that functional neuroimaging is not reliable enough, and that intrasurgical mapping is still mandatory for the detection of both eloquent cortex and functional white matter pathways; (3) the authors show a tumoral invasion of cortical areas still functional in 46.1% of cases and a tumoral invasion of subcortical structures still functional up to 34.6% of cases for language, which is a very important result supporting the necessity of performing brain mapping in glioma surgery.

However, the authors must be careful before they write that "a safe resection is feasible when only negative stimulation sites are found", because the rate of permanent deficit in their series is still of 11.1%. Indeed, the authors insisted on "learning curve" with regard to awake mapping. In this state of mind, it is important for neurosurgeons who begin this activity to remind that a perfect methodology of electrostimulation is crucial, especially to avoid false negative which could lead to permanent deficit. A positive mapping is thus highly recommended in order to have well-understood the individual anatomo-functional organization before to remove a cerebral tumor, and to tailor the resection according to these reliable boundaries which are very variable from one patient to another.

Hugues Duffau

Montpellier, France

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Spena, G., Nava, A., Cassini, F. et al. Preoperative and intraoperative brain mapping for the resection of eloquent-area tumors. A prospective analysis of methodology, correlation, and usefulness based on clinical outcomes. Acta Neurochir 152, 1835–1846 (2010). https://doi.org/10.1007/s00701-010-0764-9

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