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Combination of Multimodal MRI, Neuronavigation, and Awake Craniotomy in Removing Tumors of Eloquent Areas

Combination of Multimodal MRI, Neuronavigation, and Awake Craniotomy in Removing Tumors of Eloquent Areas

Zolotova А.S., Evstigneyev М.S., Yashin К.S., Ermolayev А.Yu., Ostapyuk М.V., Al-Madhadjy V.M.A., Zagrekov V.I., Antonova N.Yu., Shibanova М.V., Kravets L.Ya., Gronskaya N.E., Medyanik I.А.
Key words: awake craniotomy; intracerebral tumors; eloquent areas; multimodal MRI; neuronavigation.
2022, volume 14, issue 2, page 59.

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The aim of the study is to assess the possibilities of the combined approach to using multimodal MRI, neuronavigation, and awake craniotomy in resecting tumors of eloquent areas.

Materials and Methods. The results of 30 successive awake surgical interventions performed in 2017−2019 years in patients with tumors of eloquent areas have been analyzed. The main selection criterion for this type of operations was the location of the tumor in the projection or in the immediate proximity to the cortical centers of speech and motion. To minimize the damage, patients underwent functional MRI and DTI tractography at the prehospital stage to identify cortical regions and white matter tracts involved in the motor and language functions; immediately before the operation the acquired data was loaded into the navigation StealthStation S7 (Medtronic, USA) to plan and monitor surgery stages; during the surgery, direct cortical and subcortical stimulation was performed to identify the motor and speech centers (asleep−awake−asleep technique) with neurolinguistic testing. Karnofsky performance status, assessment of the patient’s neurological status, frequency of epileptic seizures before and after the operation, the extent of the tumor resection, and the data analysis after the linguistic testing were used to determine the patients’ condition and surgery outcomes.

Results. Improvement of the general state after the operation has been noted in 30% of patients compared to the preoperative condition, no neurological deficit dynamics has been observed in 33% of patients. Postoperative multimodal MRI showed that total tumor removal was achieved in 37% of cases, subtotal in 40%, partial removal resection in 23% of cases.

Conclusion. The combined approach to the brain tumor resection using multimodal MRI, neuronavigation, and awake craniotomy with motor and language areas mapping allows neurosurgeons to minimize the risk of persistent neurological deficit occurrence and provides the possibility to perform maximal resection possible preserving the patients’ functional status. The presented methodology is reproducible, permitting one to expand the options of surgical treatment when lesions are localized in eloquent areas.

  1. Kim S.S., McCutcheon I.E., Suki D., Weinberg J.S., Sawaya R., Lang F.F., Ferson D., Heimberger A.B., DeMonte F., Prabhu S.S. Awake craniotomy for brain tumors near eloquent cortex: correlation of intraoperative cortical mapping with neurological outcomes in 309 consecutive patients. Neurosurgery 2009; 64(5): 836–346,
  2. Almenawer S.A., Badhiwala J.H., Alhazzani W., Greenspoon J., Farrokhyar F., Yarascavitch B., Algird A., Kachur E., Cenic A., Sharieff W., Klurfan P., Gunnarsson T., Ajani O., Reddy K., Singh S.K., Murty N.K. Biopsy versus partial versus gross total resection in older patients with high-grade glioma: a systematic review and meta-analysis. Neuro Oncol 2015; 17(6): 868–881,
  3. Jung T.Y., Jung S., Moon J.H., Kim I.Y., Moon K.S., Jang W.Y. Early prognostic factors related to progression and malignant transformation of low-grade gliomas. Clin Neurol Neurosurg 2011; 113(9): 752–757,
  4. Zhang J.J.Y., Lee K.S., Voisin M.R., Hervey-Jumper S.L., Berger M.S., Zadeh G. Awake craniotomy for resection of supratentorial glioblastoma: a systematic review and meta-analysis. Neurooncol Adv 2020; 2(1): vdaa111,
  5. Rahman M., Abbatematteo J., De Leo E.K., Kubilis P.S., Vaziri S., Bova F., Sayour E., Mitchell D., Quinones-Hinojosa A. The effects of new or worsened postoperative neurological deficits on survival of patients with glioblastoma. J Neurosurg 2017; 127(1): 123–131,
  6. van Kessel E., Snijders T.J., Baumfalk A.E., Ruis C., van Baarsen K.M., Broekman M.L., van Zandvoort M.J.E., Robe P.A. Neurocognitive changes after awake surgery in glioma patients: a retrospective cohort study. J Neurooncol 2020; 146(1): 97–109,
  7. Kumar A., Chandra P.S., Sharma B.S., Garg A., Rath G.K., Bithal P.K., Tripathi M. The role of neuronavigation-guided functional MRI and diffusion tensor tractography along with cortical stimulation in patients with eloquent cortex lesions. Br J Neurosurg 2014; 28(2): 226–233,
  8. Whiting B.B., Lee B.S., Mahadev V., Borghei-Razavi H., Ahuja S., Jia X., Mohammadi A.M., Barnett G.H., Angelov L., Rajan S., Avitsian R., Vogelbaum M.A. Combined use of minimal access craniotomy, intraoperative magnetic resonance imaging, and awake functional mapping for the resection of gliomas in 61 patients. J Neurosurg 2019; 132(1): 159–167,
  9. Sarubbo S., Tate M., De Benedictis A., Merler S., Moritz-Gasser S., Herbet G., Duffau H. A normalized dataset of 1821 cortical and subcortical functional responses collected during direct electrical stimulation in patients undergoing awake brain surgery. Data Brief 2019; 28: 104892,
  10. Ivanova M., Dragoy O., Akinina J., Soloukhina O., Iskra E., Khudyakova M., Akhutina T. AutoRAT at your fingertips: introducing the new Russian Aphasia Test on a tablet. In: Frontiers in Psychology. Conference Abstract: 54th Annual Academy of Aphasia Meeting. Llandudno, Wales; 2016,
  11. Dragoy O., Chrabaszcz A., Tolkacheva V., Buklina S. Russian intraoperative naming test: a standardized tool to map noun and verb production during awake neurosurgeries. The Russian Journal of Cognitive Science 2016; 3(4): 4–25,
  12. Dragoy O., Zyryanov A., Bronov O., Gordeyeva E., Gronskaya N., Kryuchkova O., Klyuev E., Kopachev D., Medyanik I., Mishnyakova L., Pedyash N., Pronin I., Reutov A., Sitnikov A., Stupina E., Yashin K., Zhirnova V., Zuev A. Functional linguistic specificity of the left frontal aslant tract for spontaneous speech fluency: evidence from intraoperative language mapping. Brain Lang 2020; 208: 104836,
  13. Chang E.F., Breshears J.D., Raygor K.P., Lau D., Molinaro A.M., Berger M.S. Stereotactic probability and variability of speech arrest and anomia sites during stimulation mapping of the language dominant hemisphere. J Neurosurg 2017; 126(1): 114–121,
  14. Roux F.E., Boulanouar K., Lotterie J.A., Mejdoubi M., LeSage J.P., Berry I. Language functional magnetic resonance imaging in preoperative assessment of language areas: correlation with direct cortical stimulation. Neurosurgery 2003; 52(6): 1335–1347,
  15. De Witte E., Mariën P. The neurolinguistic approach to awake surgery reviewed. Clin Neurol Neurosurg 2013; 115(2): 127–145,
  16. Silva M.A., See A.P., Essayed W.I., Golby A.J., Tie Y. Challenges and techniques for presurgical brain mapping with functional MRI. Neuroimage Clin 2017; 17: 794–803,
  17. Rigolo L., Essayed W., Tie Y., Norton I., Mukundan S. Jr., Golby A. Intraoperative use of functional MRI for surgical decision making after limited or infeasible electrocortical stimulation mapping. J Neuroimaging 2020; 30(2): 184–191,
  18. Kapsalakis I.Z., Kapsalaki E.Z., Gotsis E.D., Verganelakis D., Toulas P., Hadjigeorgiou G., Chung I., Fezoulidis I., Papadimitriou A., Robinson J.S., Lee G.P., Fountas K.N. Preoperative evaluation with FMRI of patients with intracranial gliomas. Radiol Res Pract 2012; 2012: 727810,
  19. Weng H.H., Noll K.R., Johnson J.M., Prabhu S.S., Tsai Y.H., Chang S.W., Huang Y.C., Lee J.D., Yang J.T., Yang C.T., Tsai Y.H., Yang C.Y., Hazle J.D., Schomer D.F., Liu H.L. Accuracy of presurgical functional MR imaging for language mapping of brain tumors: a systematic review and meta-analysis. Radiology 2018; 286(2): 512–523,
  20. Lee J.J., Luckett P., Fakhri M.M., Leuthardt E.C., Shimony J.S. Resting state functional MR imaging of language function. Neuroimaging Clin N Am 2021; 31(1): 69–79,
  21. Mato D., Velasquez C., Gómez E., Marco de Lucas E., Martino J. Predicting the extent of resection in low-grade glioma by using intratumoral tractography to detect eloquent fascicles within the tumor. Neurosurgery 2021; 88(2): E190–E202,
  22. Stevanovic A., Rossaint R., Veldeman M., Bilotta F., Coburn M. Anaesthesia management for awake craniotomy: systematic review and meta-analysis. PLoS One 2016; 11(5): e0156448,
  23. Hervey-Jumper S.L., Li J., Lau D., Molinaro A.M., Perry D.W., Meng L., Berger M.S. Awake craniotomy to maximize glioma resection: methods and technical nuances over a 27-year period. J Neurosurg 2015; 123(2): 325–339,
  24. Boetto J., Bertram L., Moulinié G., Herbet G., Moritz-Gasser S., Duffau H. Low rate of intraoperative seizures during awake craniotomy in a prospective cohort with 374 supratentorial brain lesions: electrocorticography is not mandatory. World Neurosurg 2015; 84(6): 1838–1844,
  25. Gonen T., Grossman R., Sitt R., Nossek E., Yanaki R., Cagnano E., Korn A., Hayat D., Ram Z. Tumor location and IDH1 mutation may predict intraoperative seizures during awake craniotomy. J Neurosurg 2014; 121(5): 1133–1138,
  26. Szelényi A., Bello L., Duffau H., Fava E., Feigl G.C., Galanda M., Neuloh G., Signorelli F., Sala F.; Workgroup for Intraoperative Management in Low-Grade Glioma Surgery within the European Low-Grade Glioma Network. Intraoperative electrical stimulation in awake craniotomy: methodological aspects of current practice. Neurosurg Focus 2010; 28(2): E7,
  27. Akay A., Islekel S. Awake craniotomy procedure: its effects on neurological morbidity and recommendations. Turk Neurosurg 2018; 28(2): 186–192,
  28. Nossek E., Matot I., Shahar T., Barzilai O., Rapoport Y., Gonen T., Sela G., Grossman R., Korn A., Hayat D., Ram Z. Intraoperative seizures during awake craniotomy: incidence and consequences: analysis of 477 patients. Neurosurgery 2013; 73(1): 135–140,
  29. Joswig H., Bratelj D., Brunner T., Jacomet A., Hildebrandt G., Surbeck W. Awake craniotomy: first-year experiences and patient perception. World Neurosurg 2016; 90: 588–596.e2,
  30. Sanai N., Mirzadeh Z., Berger M.S. Functional outcome after language mapping for glioma resection. N Engl J Med 2008; 358(1): 18–27,
  31. Duffau H. Surgery of low-grade gliomas: towards a ‘functional neurooncology’. Curr Opin Oncol 2009; 21(6): 543–549,
  32. Aibar-Durán J.Á., de Quintana-Schmidt C., Álvarez Holzpafel M.J., Hernández F.M., Cortés C.A., Martínez G.V., Bertrán G.C. Intraoperative use and benefits of tractography in awake surgery patients. World Neurosurg 2020; 137: e347–e353,
  33. Vanderweyen D.C., Theaud G., Sidhu J., Rheault F., Sarubbo S., Descoteaux M., Fortin D. The role of diffusion tractography in refining glial tumor resection. Brain Struct Funct 2020; 225(4): 1413–1436,
  34. Henderson F., Abdullah K.G., Verma R., Brem S. Tractography and the connectome in neurosurgical treatment of gliomas: the premise, the progress, and the potential. Neurosurg Focus 2020; 48(2): E6,
  35. Pallud J., Dezamis E. Functional and oncological outcomes following awake surgical resection using intraoperative cortico-subcortical functional mapping for supratentorial gliomas located in eloquent areas. Neurochirurgie 2017; 63(3): 208–218,
  36. Rolinski R., Austermuehle A., Wiggs E., Agrawal S., Sepeta L.N., Gaillard W.D., Zaghloul K.A., Inati S.K., Theodore W.H. Functional MRI and direct cortical stimulation: prediction of postoperative language decline. Epilepsia 2019; 60(3): 560–570,
  37. Incekara F., Olubiyi O., Ozdemir A., Lee T., Rigolo L., Golby A. The value of pre- and intraoperative adjuncts on the extent of resection of hemispheric low-grade gliomas: a retrospective analysis. J Neurol Surg A Cent Eur Neurosurg 2016; 77(2): 79–87,
Zolotova А.S., Evstigneyev М.S., Yashin К.S., Ermolayev А.Yu., Ostapyuk М.V., Al-Madhadjy V.M.A., Zagrekov V.I., Antonova N.Yu., Shibanova М.V., Kravets L.Ya., Gronskaya N.E., Medyanik I.А. Combination of Multimodal MRI, Neuronavigation, and Awake Craniotomy in Removing Tumors of Eloquent Areas. Sovremennye tehnologii v medicine 2022; 14(2): 59,

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