Skip to main content

Advertisement

SpringerLink
Log in

Resection of highly language-eloquent brain lesions based purely on rTMS language mapping without awake surgery

  • Clinical Article - Brain Tumors
  • Published:
Acta Neurochirurgica Aims and scope Submit manuscript

Abstract

Background

The resection of left-sided perisylvian brain lesions harbours the risk of postoperative language impairment. Therefore the individual patient’s language distribution is investigated by intraoperative direct cortical stimulation (DCS) during awake surgery. Yet, not all patients qualify for awake surgery. Non-invasive language mapping by repetitive navigated transcranial magnetic stimulation (rTMS) has frequently shown a high correlation in comparison with the results of DCS language mapping in terms of language-negative brain regions. The present study analyses the extent of resection (EOR) and functional outcome of patients who underwent left-sided perisylvian resection of brain lesions based purely on rTMS language mapping.

Methods

Four patients with left-sided perisylvian brain lesions (two gliomas WHO III, one glioblastoma, one cavernous angioma) underwent rTMS language mapping prior to surgery. Data from rTMS language mapping and rTMS-based diffusion tensor imaging fibre tracking (DTI-FT) were transferred to the intraoperative neuronavigation system. Preoperatively, 5 days after surgery (POD5), and 3 months after surgery (POM3) clinical follow-up examinations were performed.

Results

No patient suffered from a new surgery-related aphasia at POM3. Three patients underwent complete resection immediately, while one patient required a second rTMS-based resection some days later to achieve the final, complete resection.

Conclusions

The present study shows for the first time the feasibility of successfully resecting language-eloquent brain lesions based purely on the results of negative language maps provided by rTMS language mapping and rTMS-based DTI-FT. In very select cases, this technique can provide a rescue strategy with an optimal functional outcome and EOR when awake surgery is not feasible.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Bello L, Gambini A, Castellano A, Carrabba G, Acerbi F, Fava E, Giussani C, Cadioli M, Blasi V, Casarotti A, Papagno C, Gupta AK, Gaini S, Scotti G, Falini A (2008) Motor and language DTI Fiber Tracking combined with intraoperative subcortical mapping for surgical removal of gliomas. Neuroimage 39:369–382

    Article  PubMed  Google Scholar 

  2. Berger MS, Deliganis AV, Dobbins J, Keles GE (1994) The effect of extent of resection on recurrence in patients with low grade cerebral hemisphere gliomas. Cancer 74:1784–1791

    Article  CAS  PubMed  Google Scholar 

  3. Capelle L, Fontaine D, Mandonnet E, Taillandier L, Golmard JL, Bauchet L, Pallud J, Peruzzi P, Baron MH, Kujas M, Guyotat J, Guillevin R, Frenay M, Taillibert S, Colin P, Rigau V, Vandenbos F, Pinelli C, Duffau H (2013) Spontaneous and therapeutic prognostic factors in adult hemispheric World Health Organization Grade II gliomas: a series of 1097 cases: clinical article. J Neurosurg 118:1157–1168

    Article  PubMed  Google Scholar 

  4. Chang EF, Clark A, Smith JS, Polley MY, Chang SM, Barbaro NM, Parsa AT, McDermott MW, Berger MS (2011) Functional mapping-guided resection of low-grade gliomas in eloquent areas of the brain: improvement of long-term survival. Clinical article. J Neurosurg 114:566–573

    Article  PubMed  Google Scholar 

  5. Corina DP, Gibson EK, Martin R, Poliakov A, Brinkley J, Ojemann GA (2005) Dissociation of action and object naming: evidence from cortical stimulation mapping. Hum Brain Mapp 24:1–10

    Article  PubMed  Google Scholar 

  6. Corina DP, Loudermilk BC, Detwiler L, Martin RF, Brinkley JF, Ojemann G (2010) Analysis of naming errors during cortical stimulation mapping: implications for models of language representation. Brain Lang 115:101–112

    Article  PubMed  PubMed Central  Google Scholar 

  7. De Benedictis A, Duffau H (2011) Brain hodotopy: from esoteric concept to practical surgical applications. Neurosurgery 68:1709–1723, discussion 1723

    Article  PubMed  Google Scholar 

  8. De Witt Hamer PC, Robles SG, Zwinderman AH, Duffau H, Berger MS (2012) Impact of intraoperative stimulation brain mapping on glioma surgery outcome: a meta-analysis. J Clin Oncol 30:2559–2565

    Article  PubMed  Google Scholar 

  9. De Witt Hamer PC, Hendriks EJ, Mandonnet E, Barkhof F, Zwinderman AH, Duffau H (2013) Resection probability maps for quality assessment of glioma surgery without brain location bias. PLoS One 8, e73353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Duffau H (2013) Diffusion tensor imaging is a research and educational tool, but not yet a clinical tool. World Neurosurg 82(1-2):e43-e45

  11. Duffau H (2014) The huge plastic potential of adult brain and the role of connectomics: new insights provided by serial mappings in glioma surgery. Cortex 58:325–337

    Article  PubMed  Google Scholar 

  12. Frey D, Strack V, Wiener E, Jussen D, Vajkoczy P, Picht T (2012) A new approach for corticospinal tract reconstruction based on navigated transcranial stimulation and standardized fractional anisotropy values. Neuroimage 62:1600–1609

    Article  CAS  PubMed  Google Scholar 

  13. Freyschlag CF, Duffau H (2014) Awake brain mapping of cortex and subcortical pathways in brain tumor surgery. J Neurosurg Sci 58:199–213

    CAS  PubMed  Google Scholar 

  14. Haglund MM, Berger MS, Shamseldin M, Lettich E, Ojemann GA (1994) Cortical localization of temporal lobe language sites in patients with gliomas. Neurosurgery 34:567–576, discussion 576

    Article  CAS  PubMed  Google Scholar 

  15. Henry RG, Berman JI, Nagarajan SS, Mukherjee P, Berger MS (2004) Subcortical pathways serving cortical language sites: initial experience with diffusion tensor imaging fiber tracking combined with intraoperative language mapping. Neuroimage 21:616–622

    Article  PubMed  PubMed Central  Google Scholar 

  16. Hernandez-Pavon JC, Makela N, Lehtinen H, Lioumis P, Makela JP (2014) Effects of navigated TMS on object and action naming. Front Hum Neurosci 8:660

    Article  PubMed  PubMed Central  Google Scholar 

  17. Hervey-Jumper SL, Li J, Lau D, Molinaro AM, Perry DW, Meng L, Berger MS (2015) Awake craniotomy to maximize glioma resection: methods and technical nuances over a 27-year period. J Neurosurg 123:325–339

    Article  PubMed  Google Scholar 

  18. Huber WWD, Poeck K, Willmes K (1980) Der Aachener Aphasie Test—Aufbau und Überprüfung der Konstruktion. Nervenarzt 51:475–482

    CAS  PubMed  Google Scholar 

  19. Ille S, Sollmann N, Hauck T, Maurer S, Tanigawa N, Obermueller T, Negwer C, Droese D, Boeckh-Behrens T, Meyer B, Ringel F, Krieg SM (2015) Impairment of preoperative language mapping by lesion location: a functional magnetic resonance imaging, navigated transcranial magnetic stimulation, and direct cortical stimulation study. J Neurosurg 123(2):314-324

  20. Ille S, Sollmann N, Hauck T, Maurer S, Tanigawa N, Obermueller T, Negwer C, Droese D, Zimmer C, Meyer B, Ringel F, Krieg SM (2015) Combined noninvasive language mapping by navigated transcranial magnetic stimulation and functional MRI and its comparison with direct cortical stimulation. J Neurosurg 123(1):212-225

  21. Jimenez de la Pena M, Gil Robles S, Recio Rodriguez M, Ruiz Ocana C, Martinez de Vega V (2013) Cortical and subcortical mapping of language areas: correlation of functional MRI and tractography in a 3T scanner with intraoperative cortical and subcortical stimulation in patients with brain tumors located in eloquent areas. Radiologia 55:505–513

    Article  CAS  PubMed  Google Scholar 

  22. Kinoshita M, Yamada K, Hashimoto N, Kato A, Izumoto S, Baba T, Maruno M, Nishimura T, Yoshimine T (2005) Fiber-tracking does not accurately estimate size of fiber bundle in pathological condition: initial neurosurgical experience using neuronavigation and subcortical white matter stimulation. Neuroimage 25:424–429

    Article  PubMed  Google Scholar 

  23. Kral T, Kurthen M, Schramm J, Urbach H, Meyer B (2007) Stimulation mapping via implanted grid electrodes prior to surgery for gliomas in highly eloquent cortex. Neurosurgery 61:319–325, discussion 325–316

    Article  PubMed  Google Scholar 

  24. Krieg SM, Buchmann NH, Gempt J, Shiban E, Meyer B, Ringel F (2012) Diffusion tensor imaging fiber tracking using navigated brain stimulation—a feasibility study. Acta Neurochir (Wien) 154:555–563

    Article  Google Scholar 

  25. Krieg SM, Shiban E, Buchmann N, Gempt J, Foerschler A, Meyer B, Ringel F (2012) Utility of presurgical navigated transcranial magnetic brain stimulation for the resection of tumors in eloquent motor areas. J Neurosurg 116:994–1001

    Article  PubMed  Google Scholar 

  26. Krieg SM, Sollmann N, Hauck T, Ille S, Foerschler A, Meyer B, Ringel F (2013) Functional language shift to the right hemisphere in patients with language-eloquent brain tumors. PLoS One 8, e75403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Krieg SM, Sollmann N, Hauck T, Ille S, Meyer B, Ringel F (2014) Repeated mapping of cortical language sites by preoperative navigated transcranial magnetic stimulation compared to repeated intraoperative DCS mapping in awake craniotomy. BMC Neurosci 15:20

    Article  PubMed  PubMed Central  Google Scholar 

  28. Krieg SM, Tarapore PE, Picht T, Tanigawa N, Houde J, Sollmann N, Meyer B, Vajkoczy P, Berger MS, Ringel F, Nagarajan S (2014) Optimal timing of pulse onset for language mapping with navigated repetitive transcranial magnetic stimulation. Neuroimage 100:219–236

    Article  PubMed  Google Scholar 

  29. Lacroix M, Abi-Said D, Fourney DR, Gokaslan ZL, Shi W, DeMonte F, Lang FF, McCutcheon IE, Hassenbusch SJ, Holland E, Hess K, Michael C, Miller D, Sawaya R (2001) A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J Neurosurg 95:190–198

    Article  CAS  PubMed  Google Scholar 

  30. Leclercq D, Duffau H, Delmaire C, Capelle L, Gatignol P, Ducros M, Chiras J, Lehericy S (2010) Comparison of diffusion tensor imaging tractography of language tracts and intraoperative subcortical stimulations. J Neurosurg 112:503–511

    Article  PubMed  Google Scholar 

  31. Lioumis P, Zhdanov A, Makela N, Lehtinen H, Wilenius J, Neuvonen T, Hannula H, Deletis V, Picht T, Makela JP (2012) A novel approach for documenting naming errors induced by navigated transcranial magnetic stimulation. J Neurosci Methods 204:349–354

    Article  PubMed  Google Scholar 

  32. Matsuda R, Coello AF, De Benedictis A, Martinoni M, Duffau H (2012) Awake mapping for resection of cavernous angioma and surrounding gliosis in the left dominant hemisphere: surgical technique and functional results: clinical article. J Neurosurg 117:1076–1081

    Article  PubMed  Google Scholar 

  33. Nimsky C, Ganslandt O, Merhof D, Sorensen AG, Fahlbusch R (2006) Intraoperative visualization of the pyramidal tract by diffusion-tensor-imaging-based fiber tracking. Neuroimage 30:1219–1229

    Article  PubMed  Google Scholar 

  34. Nimsky C, Ganslandt O, Hastreiter P, Wang R, Benner T, Sorensen AG, Fahlbusch R (2007) Preoperative and intraoperative diffusion tensor imaging-based fiber tracking in glioma surgery. Neurosurgery 61:178–185, discussion 186

    PubMed  Google Scholar 

  35. Ojemann GA, Whitaker HA (1978) Language localization and variability. Brain Lang 6:239–260

    Article  CAS  PubMed  Google Scholar 

  36. Ojemann G, Ojemann J, Lettich E, Berger M (1989) Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. J Neurosurg 71:316–326

    Article  CAS  PubMed  Google Scholar 

  37. Picht T, Kombos T, Gramm HJ, Brock M, Suess O (2006) Multimodal protocol for awake craniotomy in language cortex tumour surgery. Acta Neurochir (Wien) 148:127–137, discussion 137–128

    Article  CAS  Google Scholar 

  38. Picht T, Krieg SM, Sollmann N, Rosler J, Niraula B, Neuvonen T, Savolainen P, Lioumis P, Makela JP, Deletis V, Meyer B, Vajkoczy P, Ringel F (2013) A comparison of language mapping by preoperative navigated transcranial magnetic stimulation and direct cortical stimulation during awake surgery. Neurosurgery 72:808–819

    Article  PubMed  Google Scholar 

  39. Rosler J, Niraula B, Strack V, Zdunczyk A, Schilt S, Savolainen P, Lioumis P, Makela J, Vajkoczy P, Frey D, Picht T (2014) Language mapping in healthy volunteers and brain tumor patients with a novel navigated TMS system: evidence of tumor-induced plasticity. Clin Neurophysiol 125:526–536

    Article  CAS  PubMed  Google Scholar 

  40. Rossi S, Hallett M, Rossini PM, Pascual-Leone A (2009) Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 120:2008–2039

    Article  PubMed  PubMed Central  Google Scholar 

  41. Rossini PM, Burke D, Chen R, Cohen LG, Daskalakis Z, Di Iorio R, Di Lazzaro V, Ferreri F, Fitzgerald PB, George MS, Hallett M, Lefaucheur JP, Langguth B, Matsumoto H, Miniussi C, Nitsche MA, Pascual-Leone A, Paulus W, Rossi S, Rothwell JC, Siebner HR, Ugawa Y, Walsh V, Ziemann U (2015) 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 126:1071–1107

    Article  CAS  PubMed  Google Scholar 

  42. Sanai N, Berger MS (2008) Glioma extent of resection and its impact on patient outcome. Neurosurgery 62:753–764, discussion 264–756

    Article  PubMed  Google Scholar 

  43. Sanai N, Berger MS (2008) Mapping the horizon: techniques to optimize tumor resection before and during surgery. Clin Neurosurg 55:14–19

    PubMed  Google Scholar 

  44. Sanai N, Mirzadeh Z, Berger MS (2008) Functional outcome after language mapping for glioma resection. N Engl J Med 358:18–27

    Article  CAS  PubMed  Google Scholar 

  45. Sollmann N, Picht T, Makela JP, Meyer B, Ringel F, Krieg SM (2013) Navigated transcranial magnetic stimulation for preoperative language mapping in a patient with a left frontoopercular glioblastoma. J Neurosurg 118:175–179

    Article  PubMed  Google Scholar 

  46. Sollmann N, Giglhuber K, Tussis L, Meyer B, Ringel F, Krieg SM (2015) nTMS-based DTI fiber tracking for language pathways correlates with language function and aphasia—a case report. Clin Neurol Neurosurg 136:25–28

    Article  PubMed  Google Scholar 

  47. Sollmann N, Ille S, Hauck T, Maurer S, Negwer C, Zimmer C, Ringel F, Meyer B, Krieg SM (2015) The impact of preoperative language mapping by repetitive navigated transcranial magnetic stimulation on the clinical course of brain tumor patients. BMC Cancer 15:261

    Article  PubMed  PubMed Central  Google Scholar 

  48. Stummer W, Reulen HJ, Meinel T, Pichlmeier U, Schumacher W, Tonn JC, Rohde V, Oppel F, Turowski B, Woiciechowsky C, Franz K, Pietsch T (2008) Extent of resection and survival in glioblastoma multiforme: identification of and adjustment for bias. Neurosurgery 62:564–576

    Article  PubMed  Google Scholar 

  49. Tarapore PE, Findlay AM, Honma SM, Mizuiri D, Houde JF, Berger MS, Nagarajan SS (2013) Language mapping with navigated repetitive TMS: proof of technique and validation. Neuroimage 82:260–272

    Article  PubMed  Google Scholar 

  50. Tarapore PE, Picht T, Bulubas L, Shin Y, Kulchytska N, Meyer B, Berger MS, Nagarajan SS, Krieg SM (2016) Safety and tolerability of navigated TMS for preoperative mapping in neurosurgical patients. Clin Neurophysiol 127:1895–1900

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Neurosurgery, Klinikum rechts der Isar, Technische Universität München, Ismaninger Str. 22, 81675, Munich, Germany

    Sebastian Ille, Nico Sollmann, Vicki M. Butenschoen, Bernhard Meyer, Florian Ringel & Sandro M. Krieg

  2. TUM Neuroimaging Center, Klinikum rechts der Isar, Technische Universität München, Munich, Germany

    Sebastian Ille, Nico Sollmann, Vicki M. Butenschoen & Sandro M. Krieg

Authors
  1. Sebastian Ille
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nico Sollmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vicki M. Butenschoen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bernhard Meyer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Florian Ringel
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sandro M. Krieg
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sandro M. Krieg.

Ethics declarations

Funding

The study was financed by institutional grants from the Department of Neurosurgery.

Conflict of interest

B.M., F.R., and S.K. are consultants for BrainLab AG (Feldkirchen, Germany). S.K. is a consultant for Nexstim Oy (Helsinki, Finland). The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ille, S., Sollmann, N., Butenschoen, V.M. et al. Resection of highly language-eloquent brain lesions based purely on rTMS language mapping without awake surgery. Acta Neurochir 158, 2265–2275 (2016). https://doi.org/10.1007/s00701-016-2968-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00701-016-2968-0

Keywords

Search

Navigation