Features of various parts of the arcuate fasciculus mapping in patients with left hemisphere gliomas: analysis of 23 awake brain surgeries

Background. Awake craniotomy is a modern technique of neurosurgical operations allowing to preserve speech while trying to achieve maximal tumor resection. For a long time, during awake surgeries the main importance was assigned to electrostimulation of the language centers. Currently, the mapping of the long association tracts during resection of gliomas of the speech-dominant hemisphere is the necessary requirement for speech preservation.

Aim. To analyze the results of intraoperative electrostimulation of the arcuate fasciculus in comparison with magnetic resonance tractography data (MR tractography), as well as speech disorders before and after surgical interventions in patients with left hemisphere gliomas adjacent to the arcuate fasciculus who underwent awake craniotomy.

Materials and methods. Awake surgeries were performed in 23 patients aged between 19 and 67 years old (mean age 41) with left hemisphere glionas. Tumor was located in the frontal lobe in 11 patients, in the temporal lobe - in 8 patients, in the parietal lobe - in 4 patients. The malignancy grade was the following: Grade 2-7 patients, Grade 3-12 and Grade 4-4 patients. In all patients, the cortical electrophysiological stimulation to control localization of the cortical language centers and subcortical electrophysiological stimulation for identification of the arcuate fasciculus were performed during awakening. Speech disorders before and after surgery were evaluated by a neuropsychologist using the Luria method; intraoperatively, automated test with picture naming was additionally used. The mean current intensity during direct subcortical electrostimulation was 4 mA. MR tractography with reconstruction of the arcuate fasciculus and volumetry using magnetic resonance imaging (MRI) were performed in all 23 cases before and after surgery.

Results. During intraoperative electrostimulation, Broca's area was identified in 8 of 11 patients with frontal lobe tumors, cortical temporal speech areas were identified in 5 of 8 patients with temporal lobe tumors. In 16 (70 %) of 23 patients, the arcuate fasciculus was mapped in the form of mixed speech abnormalities in the depth of operative wound in the frontal, parietal and temporal lobes. In 17 (75 %) of 23 patients, worsening the speech function was observed in the early postoperative period: in 13 of them a combination of frontal and temporal types of speech disorders (conduction aphasia caused by the surgery near the arcuate fascisulus) was observed. The postoperative MR tractography performed in 23 patients showed the direct intraoperative injury of the arcuate fasciculus in 3 (13 %) cases and adjacent ischemia - in 2 (9 %) cases. The MR volumetry showed total tumor resection in 8 cases, subtotal - in 9 cases, and partial - in 6 cases.

Conclusion. During awake surgeries for left hemisphere tumors, it is important to map the arcuate fasciculus in the deep parts of the frontal, temporal and parietal lobes. The subcortical stimulation allowed to identify the arcuate fasciculus in 70 % of presented cases; the MR tractography showed the damage of the anatomical integrity of the arcuate fasciculus in 22 % of cases (direct injury or ischemia). Worsened speech function after surgery was observed in 75 % of patients. In the early postoperative period, the main cause of worsened speech function related to the arcuate fasciculus is its functional insufficiency but not an anatomical damage. These speech disorders regress in the majority of patients (85 %) in 3-6 months after surgery.

1. Larjavaara S., Mäntylä R., Salminen T. et al. Incidence of gliomas by anatomic location. Neuro Oncol 2007;9(3):319-25. DOI: 10.1215/15228517-2007-016

2. Sanai N., Mirzadeh Z., Berger M.S. Functional outcome after language mapping for glioma resection. N Engl J Med 2008;358(1):18-27. DOI: 10.1056/NEJMoa067819

3. Aabedi A.A., Young J.S., Chang E.F. et al. Involvement of white matter language tracts in glioma: clinical implications, operative management, and functional recovery after injury. Front Neurosci 2022;16:932478. DOI: 10.3389/fnins.2022.932478

4. Bello L., Gambini A., Castellano A. et al. Motor and language DTI Fiber Tracking combined with intraoperative subcortical mapping for surgical removal of gliomas. Neuroimage 2008;39(1):369-82. DOI: 10.1016/j.neuroimage.2007.08.031

5. Zhukov V.Yu., Goryainov S.A., Buklina S.B. et al. Mapping of cortical speech zones and arcuate tract in patients with gliomas of temporal lobe of left hemisphere (analysis of a series of 27 observations). Neyrokhirurgiya = Russian Journal of Neurosurgery 2023;25(1):53-61. DOI: 10.17650/1683-3295-2023-25-1-53-61

6. Goriaynov S.A., Kondrashov A.V., Goldberg M.F. et al. Long association tracts of the human white matter: an analysis of 18 hemisphere dissections and in vivo HARDI-CSD tractography. Zhurnal Voprosy neyrokhururgii im. N.N. Burdenko = Burdenko ’ s Journal of Neurosurger 2017;81(1):13-25. (in Russ., in Engl.). DOI: 10.17116/neiro201780713-25

7. Zhukov V.Yu., Goriaynov S.A., Buklina S.B. et al. Intraoperative mapping of long association fibers in surgery of gliomas of the speech-dominant frontal lobe. Zhurnal Voprosy neyrokhururgii im. N.N. Burdenko = Burdenko's Journal of Neurosurgery 2018;82(5):5-20. (in Russ., in Engl.). DOI: 10.17116/neiro2018820515

8. Luria A.R. Disorders of higher cortical functions in focal brain lesions. Moscow: Izd-vo MGU, 1962. 432 p.

9. Dragoy O., Chrabaszcz A., Tolkacheva V., Buklina S.B. Russian intraoperative naming Test: a standardized tool to map noun and verb production during awake neurosurgeries. Russian Journal of Cognitive Sciences 2016;3(4):4-25. DOI: 10.47010/16.4.1

10. Anderson J.M., Gilmore R., Roper S. et al. Conduction aphasia and the arcuate fasciculus: a reexamination of the Wernicke-Geschwind model. Brain lang 1999;70(1):1-12. DOI: 10.24835/1607-0763-109

11. Zöllner J.P., Haag A., Hermsen A. et al. Ictal conduction aphasia and ictal angular gyrus syndrome as rare manifestations of epilepsy: the importance of ictal testing during video-EEG monitoring. Epilepsy Behav Case Rep 2017;8:55-62. DOI: 10.1016/j.ebcr.2017.07.003

12. Mato D., Velasquez C., Gomez E. et al. 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. DOI: 10.1093/neuros/nyaa463

13. Rolston J.D., Englot D.J., Benet A. et al. Frontal operculum gliomas: language outcome following resection. J Neurosurg 2015;122(4):725-34. DOI: 10.3171/2014.11.JNS132172

14. Duffau H., Gatignol P., Mandonnet E. et al. 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(3):461-71. DOI: 10.3171/JNS/2008/109/9/0461

15. Manfield J., Waqar M., Mercer D. et al. Multimodal mapping and monitoring is beneficial during awake craniotomy for intra-cranial tumours: results of a dual centre retrospective study. Br J Neurosurg 2023;37(2):182-7. DOI: 10.1080/02688697.2021.2016622

16. Potapov A.A., Goriaynov S.A., Zhukov V.Yu. et al. The long- associative pathways of the white matter: modern view from the perspective of neuroscience. Zhurnal Voprosy neyrokhururgii im. N.N. Burdenko = Burdenko’s Journal of Neurosurgery 2014;78(5):66-77. (in Russ., in Engl.).

17. Brown T., Shah A.H., Bregy A. et al. Awake craniotomy for brain tumor resection: the rule rather than the exception? J Neurosurg anesthesiol 2013;25(3):240-7. DOI: 10.1097/ANA.0b013e318290c230

18. Andrews J., Cahn N., Speidel B. et al. Dissociation of Broca’s area from Broca’s aphasia in patients undergoing neurosurgical resections. J Neurosurg 2022;138(3):847-57. DOI: 10.3171/2022.6.JNS2297

19. Buklina S.B., Zhukov V.Yu., Goryainov S.A. et al. Conduction aphasia in patients with glioma in the left hemisphere. Zhurnal Voprosy neyrokhururgii im. N.N. Burdenko = Burdenko’s Journal of Neurosurgery 2021;85(4):29-40. (in Russ., in Engl.). DOI: 10.17116/neiro20218504129