J Neurol Surg A Cent Eur Neurosurg 2021; 82(04): 333-343
DOI: 10.1055/s-0040-1709729
Original Article

Pre- and Intraoperative Mapping for Tumors in the Primary Motor Cortex: Decision-Making Process in Surgical Resection

José Pedro Lavrador
1   Department of Neurosurgery, King's College Hospital NHS Foundation Trust, London, United Kingdom
,
1   Department of Neurosurgery, King's College Hospital NHS Foundation Trust, London, United Kingdom
,
Christian Brogna
1   Department of Neurosurgery, King's College Hospital NHS Foundation Trust, London, United Kingdom
,
Luciano Furlanetti
1   Department of Neurosurgery, King's College Hospital NHS Foundation Trust, London, United Kingdom
,
Sabina Patel
1   Department of Neurosurgery, King's College Hospital NHS Foundation Trust, London, United Kingdom
,
Richard Gullan
1   Department of Neurosurgery, King's College Hospital NHS Foundation Trust, London, United Kingdom
,
Keyoumars Ashkan
1   Department of Neurosurgery, King's College Hospital NHS Foundation Trust, London, United Kingdom
,
Ranjeev Bhangoo
1   Department of Neurosurgery, King's College Hospital NHS Foundation Trust, London, United Kingdom
,
Francesco Vergani
1   Department of Neurosurgery, King's College Hospital NHS Foundation Trust, London, United Kingdom
› Author Affiliations
Funding No funding was obtained for the study.

Abstract

Background Lesions within the primary motor cortex (M1) and the corticospinal tract (CST) represent a significant surgical challenge with a delicate functional trade-off that should be integrated in the overall patient-centered treatment plan.

Methods Patients with lesions within the M1 and CST with preoperative cortical and subcortical mapping (navigated transcranial magnetic stimulation [nTMS] and tractography), intraoperative mapping, and intraoperative provisional histologic information (smear with and without 5-aminolevulinic acid [5-ALA]) were included. This independently acquired information was integrated in a decision-making process model to determine the intraoperative extent of resection.

Results A total of 10 patients (6 patients with metastatic precentral tumor; 1 patient with grade III and 2 patients with grade IV gliomas; 1 patient with precentral cavernoma) were included in the study. Most of the patients (60%) had a preoperative motor deficit. The nTMS documented M1 invasion in all cases, and in eight patients, the lesions were embedded within the CST. Overall, 70% of patients underwent gross total resection; 20% of patients underwent near-total resection of the lesions. In only one patient was no surgical resection possible after both preoperative and intraoperative mapping. Overall, 70% of patients remained stable postoperatively, and previous motor weakness improved in 20%.

Conclusion The independently acquired anatomical (anatomical MRI) and functional (nTMS and tractography) tests in patients with CST lesions provide a useful guide for resection. The inclusion of histologic information (smear with or without 5-ALA) further allows the surgical team to balance the potential functional risks within the global treatment plan. Therefore, the patient is kept at the center of the informed decision-making process.



Publication History

Received: 25 March 2019

Accepted: 30 July 2019

Article published online:
21 May 2020

© 2020. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References

  • 1 Raffa G, Conti A, Scibilia A. et al. The impact of diffusion tensor imaging fiber tracking of the corticospinal tract based on navigated transcranial magnetic stimulation on surgery of motor-eloquent brain lesions. Neurosurgery 2018; 83 (04) 768-782
  • 2 Jung J, Lavrador JP, Patel S. et al. First United Kingdom experience of navigated transcranial magnetic stimulation in preoperative mapping of brain tumors. World Neurosurg 2019; 122: e1578-e1587
  • 3 Picht T, Schulz J, Hanna M, Schmidt S, Suess O, Vajkoczy P. Assessment of the influence of navigated transcranial magnetic stimulation on surgical planning for tumors in or near the motor cortex. Neurosurgery 2012; 70 (05) 1248-1256 ; discussion 1256–1257
  • 4 Bagić AI, Bowyer SM, Kirsch HE, Funke ME, Burgess RC. ; ACMEGS Position Statement Committee. American Clinical MEG Society (ACMEGS) Position Statement #2: The Value of Magnetoencephalography (MEG)/Magnetic Source Imaging (MSI) in Noninvasive Presurgical Mapping of Eloquent Cortices of Patients Preparing for Surgical Interventions. J Clin Neurophysiol 2017; 34 (03) 189-195
  • 5 Stevens MT, Clarke DB, Stroink G, Beyea SD, D'Arcy RC. Improving fMRI reliability in presurgical mapping for brain tumours. J Neurol Neurosurg Psychiatry 2016; 87 (03) 267-274
  • 6 D'Andrea G, Trillo' G, Picotti V, Raco A. Functional magnetic resonance imaging (fMRI), pre-intraoperative tractography in neurosurgery: the experience of Sant' Andrea Rome University Hospital. Acta Neurochir Suppl (Wien) 2017; 124: 241-250
  • 7 Tyndall AJ, Reinhardt J, Tronnier V, Mariani L, Stippich C. Presurgical motor, somatosensory and language fMRI: technical feasibility and limitations in 491 patients over 13 years. Eur Radiol 2017; 27 (01) 267-278
  • 8 Weiss Lucas C, Tursunova I, Neuschmelting V. et al. Functional MRI vs. navigated TMS to optimize M1 seed volume delineation for DTI tractography. A prospective study in patients with brain tumours adjacent to the corticospinal tract. Neuroimage Clin 2016; 13: 297-309
  • 9 Sair HI, Yahyavi-Firouz-Abadi N, Calhoun VD. et al. Presurgical brain mapping of the language network in patients with brain tumors using resting-state fMRI: comparison with task fMRI. Hum Brain Mapp 2016; 37 (03) 913-923
  • 10 Leuthardt EC, Allen M, Kamran M. et al. Resting-state blood oxygen level-dependent functional MRI: a paradigm shift in preoperative brain mapping. Stereotact Funct Neurosurg 2015; 93 (06) 427-439
  • 11 Picht T, Mularski S, Kuehn B, Vajkoczy P, Kombos T, Suess O. Navigated transcranial magnetic stimulation for preoperative functional diagnostics in brain tumor surgery. Neurosurgery 2009; 65: 93-98 (6, Suppl): discussion 98–99
  • 12 Krieg SM, Shiban E, Buchmann N. et al. Utility of presurgical navigated transcranial magnetic brain stimulation for the resection of tumors in eloquent motor areas. J Neurosurg 2012; 116 (05) 994-1001
  • 13 Tarapore PE, Findlay AM, Honma SM. et al. Language mapping with navigated repetitive TMS: proof of technique and validation. Neuroimage 2013; 82: 260-272
  • 14 Rossini PM, Burke D, Chen R. et al. Non-invasive electrical and magnetic stimulation of the brain, spinal cord, roots and peripheral nerves: basic principles and procedures for routine clinical and research application. An updated report from an I.F.C.N. Committee. Clin Neurophysiol 2015; 126 (06) 1071-1107
  • 15 Coburger J, Musahl C, Henkes H. et al. Comparison of navigated transcranial magnetic stimulation and functional magnetic resonance imaging for preoperative mapping in rolandic tumor surgery. Neurosurg Rev 2013; 36 (01) 65-75 ; discussion 75–76
  • 16 Frey D, Schilt S, Strack V. et al. Navigated transcranial magnetic stimulation improves the treatment outcome in patients with brain tumors in motor eloquent locations. Neuro Oncol 2014; 16 (10) 1365-1372
  • 17 Raffa G, Scibilia A, Conti A. et al. The role of navigated transcranial magnetic stimulation for surgery of motor-eloquent brain tumors: a systematic review and meta-analysis. Clin Neurol Neurosurg 2019; 180: 7-17
  • 18 Innocenti GM, Dyrby TB, Girard G. et al. Topological principles and developmental algorithms might refine diffusion tractography. Brain Struct Funct 2019; 224 (01) 1-8
  • 19 Campbell JS, Pike GB. Potential and limitations of diffusion MRI tractography for the study of language. Brain Lang 2014; 131: 65-73
  • 20 Catani M, Thiebaut de Schotten M. A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex 2008; 44 (08) 1105-1132
  • 21 Essayed WI, Zhang F, Unadkat P, Cosgrove GR, Golby AJ, O'Donnell LJ. White matter tractography for neurosurgical planning: a topography-based review of the current state of the art. Neuroimage Clin 2017; 15: 659-672
  • 22 Panesar SS, Abhinav K, Yeh FC, Jacquesson T, Collins M, Fernandez-Miranda J. Tractography for surgical neuro-oncology planning: towards a gold standard. Neurotherapeutics 2019; 16 (01) 36-51
  • 23 Javadi SA, Nabavi A, Giordano M, Faghihzadeh E, Samii A. Evaluation of diffusion tensor imaging-based tractography of the corticospinal tract: a correlative study with intraoperative magnetic resonance imaging and direct electrical subcortical stimulation. Neurosurgery 2017; 80 (02) 287-299
  • 24 Ohue S, Kohno S, Inoue A. et al. Surgical results of tumor resection using tractography-integrated navigation-guided fence-post catheter techniques and motor-evoked potentials for preservation of motor function in patients with glioblastomas near the pyramidal tracts. Neurosurg Rev 2015; 38 (02) 293-306 ; discussion 306–307
  • 25 Rech F, Herbet G, Moritz-Gasser S, Duffau H. Somatotopic organization of the white matter tracts underpinning motor control in humans: an electrical stimulation study. Brain Struct Funct 2016; 221 (07) 3743-3753
  • 26 Spena G, Schucht P, Seidel K. et al. Brain tumors in eloquent areas: a European multicenter survey of intraoperative mapping techniques, intraoperative seizures occurrence, and antiepileptic drug prophylaxis. Neurosurg Rev 2017; 40 (02) 287-298
  • 27 Bello L, Riva M, Fava E. et al. Tailoring neurophysiological strategies with clinical context enhances resection and safety and expands indications in gliomas involving motor pathways. Neuro Oncol 2014; 16 (08) 1110-1128
  • 28 Moiyadi A, Velayutham P, Shetty P. et al. Combined motor evoked potential monitoring and subcortical dynamic mapping in motor eloquent tumors allows safer and extended resections. World Neurosurg 2018; 120: e259-e268
  • 29 Raabe A, Beck J, Schucht P, Seidel K. Continuous dynamic mapping of the corticospinal tract during surgery of motor eloquent brain tumors: evaluation of a new method. J Neurosurg 2014; 120 (05) 1015-1024
  • 30 Shiban E, Krieg SM, Obermueller T, Wostrack M, Meyer B, Ringel F. Continuous subcortical motor evoked potential stimulation using the tip of an ultrasonic aspirator for the resection of motor eloquent lesions. J Neurosurg 2015; 123 (02) 301-306
  • 31 Schucht P, Seidel K, Beck J. et al. Intraoperative monopolar mapping during 5-ALA-guided resections of glioblastomas adjacent to motor eloquent areas: evaluation of resection rates and neurological outcome. Neurosurg Focus 2014; 37 (06) E16
  • 32 Dias S, Sarnthein J, Jehli E, Neidert MC, Regli L, Bozinov O. Safeness and utility of concomitant intraoperative monitoring with intraoperative magnetic resonance imaging in children: a pilot study. World Neurosurg 2018; 115: e637-e644
  • 33 Sollmann N, Wildschuetz N, Kelm A. et al. Associations between clinical outcome and navigated transcranial magnetic stimulation characteristics in patients with motor-eloquent brain lesions: a combined navigated transcranial magnetic stimulation-diffusion tensor imaging fiber tracking approach. J Neurosurg 2018; 128 (03) 800-810
  • 34 Weiss C, Tursunova I, Neuschmelting V. et al. Improved nTMS- and DTI-derived CST tractography through anatomical ROI seeding on anterior pontine level compared to internal capsule. Neuroimage Clin 2015; 7: 424-437
  • 35 Staempfli P, Reischauer C, Jaermann T, Valavanis A, Kollias S, Boesiger P. Combining fMRI and DTI: a framework for exploring the limits of fMRI-guided DTI fiber tracking and for verifying DTI-based fiber tractography results. Neuroimage 2008; 39 (01) 119-126
  • 36 Pujol S, Wells W, Pierpaoli C. et al. The DTI challenge: toward standardized evaluation of diffusion tensor imaging tractography for neurosurgery. J Neuroimaging 2015; 25 (06) 875-882
  • 37 Raffa G, Conti A, Scibilia A. et al. Functional reconstruction of motor and language pathways based on navigated transcranial magnetic stimulation and DTI fiber tracking for the preoperative planning of low grade glioma surgery: a new tool for preservation and restoration of eloquent networks. Acta Neurochir Suppl (Wien) 2017; 124: 251-261
  • 38 Rosenstock T, Giampiccolo D, Schneider H. et al. Specific DTI seeding and diffusivity-analysis improve the quality and prognostic value of TMS-based deterministic DTI of the pyramidal tract. Neuroimage Clin 2017; 16: 276-285
  • 39 Conti A, Raffa G, Granata F, Rizzo V, Germanò A, Tomasello F. Navigated transcranial magnetic stimulation for “somatotopic” tractography of the corticospinal tract. Neurosurgery 2014; 10 (04, Suppl 4):; discussion 554 542-554
  • 40 Ghimire P, Bedussa N, Giamouriadis A. et al. Somatotopy of corticospinal tract fibres of the intercostal muscles: report of a case and review of literature. Brain Struct Funct 2019; 224 (02) 515-520
  • 41 Zelitzki R, Korn A, Arial E, Ben-Harosh C, Ram Z, Grossman R. Comparison of motor outcome in patients undergoing awake vs general anesthesia surgery for brain tumors located within or adjacent to the motor pathways. Neurosurgery 2019; 85 (03) E470-E476
  • 42 Magill ST, Han SJ, Li J, Berger MS. Resection of primary motor cortex tumors: feasibility and surgical outcomes. J Neurosurg 2018; 129 (04) 961-972
  • 43 Adhikary SD, Thiruvenkatarajan V, Babu KS, Tharyan P. The effects of anaesthetic agents on cortical mapping during neurosurgical procedures involving eloquent areas of the brain. Cochrane Database Syst Rev 2011; (11) CD006679
  • 44 Ott C, Kerscher C, Luerding R. et al. The impact of sedation on brain mapping: a prospective, interdisciplinary, clinical trial. Neurosurgery 2014; 75 (02) 117-123 ; discussion 123; quiz 123
  • 45 Eseonu CI, Rincon-Torroella J, ReFaey K. et al. Awake craniotomy vs craniotomy under general anesthesia for perirolandic gliomas: evaluating perioperative complications and extent of resection. Neurosurgery 2017; 81 (03) 481-489
  • 46 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 2013; 118 (02) 287-296
  • 47 Mat Zin AA, Zulkarnain S. Diagnostic accuracy of cytology smear and frozen section in glioma. Asian Pac J Cancer Prev 2019; 20 (02) 321-325
  • 48 Nanarng V, Jacob S, Mahapatra D, Mathew JE. Intraoperative diagnosis of central nervous system lesions: comparison of squash smear, touch imprint, and frozen section. J Cytol 2015; 32 (03) 153-158
  • 49 Rosenstock T, Grittner U, Acker G. et al. Risk stratification in motor area-related glioma surgery based on navigated transcranial magnetic stimulation data. J Neurosurg 2017; 126 (04) 1227-1237
  • 50 Qazi AA, Radmanesh A, O'Donnell L. et al. Resolving crossings in the corticospinal tract by two-tensor streamline tractography: Method and clinical assessment using fMRI. Neuroimage 2009; 47 (Suppl. 02) T98-T106
  • 51 Plans G, Fernández-Conejero I, Rifà-Ros X, Fernández-Coello A, Rosselló A, Gabarrós A. Evaluation of the high-frequency monopolar stimulation technique for mapping and monitoring the corticospinal tract in patients with supratentorial gliomas. a proposal for intraoperative management based on neurophysiological data analysis in a series of 92 patients. Neurosurgery 2017; 81 (04) 585-594
  • 52 Patel CK, Vemaraju R, Glasbey J. et al. Trends in peri-operative performance status following resection of high grade glioma and brain metastases: The impact on survival. Clin Neurol Neurosurg 2018; 164: 67-71
  • 53 Malakhov N, Lee A, Garay E, Becker DJ, Schreiber D. Patterns of care and outcomes for glioblastoma in patients with poor performance status. J Clin Neurosci 2018; 52: 66-70