J Neurol Surg A Cent Eur Neurosurg 2021; 82(04): 344-356
DOI: 10.1055/s-0040-1717111
Original Article

Multimodal Surgical Management of Cerebral Lesions in Motor-Eloquent Areas Combining Intraoperative 3D Ultrasound with Neurophysiological Mapping

1   Department of Neurosurgery, Azienda Ospedaliero Universitaria di Sassari, Sassari, Italy
,
Stefano Ticca
1   Department of Neurosurgery, Azienda Ospedaliero Universitaria di Sassari, Sassari, Italy
,
Giosuè Dipellegrini
1   Department of Neurosurgery, Azienda Ospedaliero Universitaria di Sassari, Sassari, Italy
,
Artan Doda
1   Department of Neurosurgery, Azienda Ospedaliero Universitaria di Sassari, Sassari, Italy
,
Giampiero Muggianu
1   Department of Neurosurgery, Azienda Ospedaliero Universitaria di Sassari, Sassari, Italy
,
Riccardo Boccaletti
1   Department of Neurosurgery, Azienda Ospedaliero Universitaria di Sassari, Sassari, Italy
› Author Affiliations
Funding No funding was received for this research.

Abstract

Background Resection of tumors adjacent to motor pathways carries risks of both postoperative motor deficit and incomplete resection. Our aim was to assess usefulness and limitations of a multimodal strategy that combines intraoperative ultrasound (iUS) guided resection with intraoperative neurophysiology.

Methodology This is a prospective study of 25 patients with brain lesions adjacent to motor areas who underwent intracranial surgery with assistance of the iUS guidance system and intraoperative neurophysiological monitoring and mapping. Pathologies treated included 19 gliomas, 3 metastases, 1 anaplastic meningioma, 1 arteriovenous malformation (AVM), and 1 ependymoma. The iUS-guided lesion removal accuracy and the extent of resection were estimated and compared with a 30-day postoperative brain MRI. The results were assessed considering the extent of resection related to 6-month motor function outcome.

Results iUS was accurate in checking the extent of resection in 17 patients, whereas in 8 cases the decline of the iUS images quality did not allow a valuable assessment. Positive mapping was obtained in 16 patients. Gross total resection was achieved in 16 patients. In five of nine cases with subtotal resection, surgery was stopped because a functional area was reached. In four patients, tumor removal was limited due to the difficulty of identifying neoplastic tissue. Motor function worsening was transient in six patients and permanent in two.

Conclusions The integrated use of intraoperative neuromonitoring to identify motor areas and iUS to identify tumor–tissue interface could help increase the rate of radical resection respecting the eloquent areas.

Informed Consent

All the patients enrolled in the study provided their written consent for anonymous data collection and inclusion in the study




Publication History

Received: 26 September 2019

Accepted: 13 February 2020

Article published online:
22 December 2020

© 2020. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References

  • 1 Berger MS. Functional mapping-guided resection of low-grade gliomas. Clin Neurosurg 1995; 42: 437-452
  • 2 Carrabba G, Fava E, Giussani C. et al. Cortical and subcortical motor mapping in rolandic and perirolandic glioma surgery: impact on postoperative morbidity and extent of resection. J Neurosurg Sci 2007; 51 (02) 45-51
  • 3 Chang EF, Clark A, Smith JS. et al. Functional mapping-guided resection of low-grade gliomas in eloquent areas of the brain: improvement of long-term survival. Clinical article. J Neurosurg 2011; 114 (03) 566-573
  • 4 De Witt Hamer PC, Robles SG, Zwinderman AH, Duffau H, Berger MS. Impact of intraoperative stimulation brain mapping on glioma surgery outcome: a meta-analysis. J Clin Oncol 2012; 30 (20) 2559-2565
  • 5 Duffau H. Lessons from brain mapping in surgery for low-grade glioma: insights into associations between tumour and brain plasticity. Lancet Neurol 2005; 4 (08) 476-486
  • 6 Duffau H, Peggy Gatignol ST, Mandonnet E, Capelle L, Taillandier L. Intraoperative subcortical stimulation mapping of language pathways in a consecutive series of 115 patients with grade II glioma in the left dominant hemisphere. J Neurosurg 2008; 109 (03) 461-471
  • 7 Duffau H, Lopes M, Arthuis F. et al. Contribution of intraoperative electrical stimulations in surgery of low grade gliomas: a comparative study between two series without (1985-96) and with (1996-2003) functional mapping in the same institution. J Neurol Neurosurg Psychiatry 2005; 76 (06) 845-851 Review
  • 8 Keles GE, Lundin DA, Lamborn KR, Chang EF, Ojemann G, Berger MS. Intraoperative subcortical stimulation mapping for hemispherical perirolandic gliomas located within or adjacent to the descending motor pathways and assessment of functional outcome in 294 patients. J Neurosurg 2004; 100 (03) 369-375
  • 9 Sanai N, Berger MS. Intraoperative stimulation techniques for functional pathway preservation and glioma resection. Neurosurg Focus 2010; 28 (02) E1
  • 10 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
  • 11 Gronningsaeter A, Kleven A, Ommedal S. et al. SonoWand, an ultrasound-based neuronavigation system. Neurosurgery 2000; 47 (06) 1373-1379 , discussion 1379–1380
  • 12 Policicchio D, Doda A, Sgaramella E, Ticca S, Veneziani Santonio F, Boccaletti R. Ultrasound-guided brain surgery: echographic visibility of different pathologies and surgical applications in neurosurgical routine. Acta Neurochir (Wien) 2018; 160 (06) 1175-1185
  • 13 Mair R, Heald J, Poeata I, Ivanov M. A practical grading system of ultrasonographic visibility for intracerebral lesions. Acta Neurochir (Wien) 2013; 155 (12) 2293-2298
  • 14 Szelényi A, Senft C, Jardan M. et al. Intra-operative subcortical electrical stimulation: a comparison of two methods. Clin Neurophysiol 2011; 122 (07) 1470-1475
  • 15 Taniguchi M, Cedzich C, Schramm J. Modification of cortical stimulation for motor evoked potentials under general anesthesia: technical description. Neurosurgery 1993; 32 (02) 219-226
  • 16 Nossek E, Korn A, Shahar T. et al. Intraoperative mapping and monitoring of the corticospinal tracts with neurophysiological assessment and 3-dimensional ultrasonography-based navigation. Clinical article. J Neurosurg 2011; 114 (03) 738-746
  • 17 Ohue S, Kohno S, Inoue A. et al. Accuracy of diffusion tensor magnetic resonance imaging-based tractography for surgery of gliomas near the pyramidal tract: a significant correlation between subcortical electrical stimulation and postoperative tractography. Neurosurgery 2012; 70 (02) 283-293 , discussion 294
  • 18 Prabhu SS, Gasco J, Tummala S, Weinberg JS, Rao G. Intraoperative magnetic resonance imaging-guided tractography with integrated monopolar subcortical functional mapping for resection of brain tumors. Clinical article. J Neurosurg 2011; 114 (03) 719-726
  • 19 Kim SS, McCutcheon IE, Suki D. et al. Awake craniotomy for brain tumors near eloquent cortex: correlation of intraoperative cortical mapping with neurological outcomes in 309 consecutive patients. Neurosurgery 2009; 64 (05) 836-845 , discussion 345–346
  • 20 Sanai N, Mirzadeh Z, Berger MS. Functional outcome after language mapping for glioma resection. N Engl J Med 2008; 358 (01) 18-27
  • 21 Maesawa S, Fujii M, Nakahara N, Watanabe T, Wakabayashi T, Yoshida J. Intraoperative tractography and motor evoked potential (MEP) monitoring in surgery for gliomas around the corticospinal tract. World Neurosurg 2010; 74 (01) 153-161
  • 22 Sala F, Lanteri P. Brain surgery in motor areas: the invaluable assistance of intraoperative neurophysiological monitoring. J Neurosurg Sci 2003; 47 (02) 79-88
  • 23 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
  • 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 2013; 118 (02) 287-296
  • 25 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
  • 26 Schucht P, Seidel K, Jilch A, Beck J, Raabe A. A review of monopolar motor mapping and a comprehensive guide to continuous dynamic motor mapping for resection of motor eloquent brain tumors. Neurochirurgie 2017; 63 (03) 175-180
  • 27 Opoku-Darko M, Amuah JE, Kelly JJP. Surgical resection of anterior and posterior butterfly glioblastoma. World Neurosurg 2018; 110: e612-e620
  • 28 Skirboll SS, Ojemann GA, Berger MS, Lettich E, Winn HR. Functional cortex and subcortical white matter located within gliomas. Neurosurgery 1996; 38 (04) 678-684 , discussion 684–685
  • 29 Eisner W, Burtscher J, Bale R. et al. Use of neuronavigation and electrophysiology in surgery of subcortically located lesions in the sensorimotor strip. J Neurol Neurosurg Psychiatry 2002; 72 (03) 378-381
  • 30 Chacko AG, Kumar NK, Chacko G, Athyal R, Rajshekhar V. Intraoperative ultrasound in determining the extent of resection of parenchymal brain tumours: a comparative study with computed tomography and histopathology. Acta Neurochir (Wien) 2003; 145 (09) 743-748 , discussion 748
  • 31 Rygh OM, Selbekk T, Torp SH, Lydersen S, Hernes TA, Unsgaard G. Comparison of navigated 3D ultrasound findings with histopathology in subsequent phases of glioblastoma resection. Acta Neurochir (Wien) 2008; 150 (10) 1033-1041 , discussion 1042
  • 32 Sæther CA, Torsteinsen M, Torp SH, Sundstrøm S, Unsgård G, Solheim O. Did survival improve after the implementation of intraoperative neuronavigation and 3D ultrasound in glioblastoma surgery? A retrospective analysis of 192 primary operations. J Neurol Surg A Cent Eur Neurosurg 2012; 73 (02) 73-78
  • 33 Solheim O, Selbekk T, Jakola AS, Unsgård G. Ultrasound-guided operations in unselected high-grade gliomas: overall results, impact of image quality and patient selection. Acta Neurochir (Wien) 2010; 152 (11) 1873-1886
  • 34 Unsgaard G, Rygh OM, Selbekk T. et al. Intra-operative 3D ultrasound in neurosurgery. Acta Neurochir (Wien) 2006; 148 (03) 235-253 , discussion 253
  • 35 Unsgaard G, Selbekk T, Brostrup Müller T. et al. Ability of navigated 3D ultrasound to delineate gliomas and metastases: comparison of image interpretations with histopathology. Acta Neurochir (Wien) 2005; 147 (12) 1259-1269 , discussion 1269
  • 36 Woydt M, Krone A, Becker G, Schmidt K, Roggendorf W, Roosen K. Correlation of intra-operative ultrasound with histopathologic findings after tumour resection in supratentorial gliomas. A method to improve gross total tumour resection. Acta Neurochir (Wien) 1996; 138 (12) 1391-1398
  • 37 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
  • 38 Feigl GC, Ritz R, Moraes M. et al. Resection of malignant brain tumors in eloquent cortical areas: a new multimodal approach combining 5-aminolevulinic acid and intraoperative monitoring. J Neurosurg 2010; 113 (02) 352-357
  • 39 Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F, Reulen HJ. ALA-Glioma Study Group. Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol 2006; 7 (05) 392-401
  • 40 Suero Molina E, Schipmann S, Stummer W. Maximizing safe resections: the roles of 5-aminolevulinic acid and intraoperative MR imaging in glioma surgery-review of the literature. Neurosurg Rev 2019; 42 (02) 197-208
  • 41 Coburger J, Nabavi A, König R, Wirtz CR, Pala A. Contemporary use of intraoperative imaging in glioma surgery: a survey among EANS members. Clin Neurol Neurosurg 2017; 163: 133-141
  • 42 Roder C, Bisdas S, Ebner FH. 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 2014; 40 (03) 297-304
  • 43 Schucht P, Beck J, Raabe A. Response to: “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 2015; 41 (04) 604-605
  • 44 Coburger J, Wirtz CR. Fluorescence guided surgery by 5-ALA and intraoperative MRI in high grade glioma: a systematic review. J Neurooncol 2019; 141 (03) 533-546
  • 45 Coburger J, Scheuerle A, Pala A, Thal D, Wirtz CR, König R. Histopathological insights on imaging results of intraoperative magnetic resonance imaging, 5-aminolevulinic acid, and intraoperative ultrasound in glioblastoma surgery. Neurosurgery 2017; 81 (01) 165-174
  • 46 Zhuang DX, Wu JS, Yao CJ. et al. Intraoperative multi-information-guided resection of dominant-sided insular gliomas in a 3-T intraoperative magnetic resonance imaging integrated neurosurgical suite. World Neurosurg 2016; 89: 84-92
  • 47 Seidel K, Beck J, Stieglitz L, Schucht P, Raabe A. Low-threshold monopolar motor mapping for resection of primary motor cortex tumors. Neurosurgery 2012;71(01), Suppl Operative ):104–114, discussion 114–115