Function-guided Differences of Arcuate Fascicle and Inferior Fronto-occipital Fascicle Tractography As Diagnostic Indicators for Surgical Risk Stratification

Overview

Journal Brain Struct Funct

Specialty Neurology

Date 2024 Apr 10

PMID 38597941

Authors

Leonie Kram

Axel Schroeder

Bernhard Meyer

Sandro M Krieg

Sebastian Ille

Affiliations

Soon will be listed here.

Abstract

Background: Several patients with language-eloquent gliomas face language deterioration postoperatively. Persistent aphasia is frequently associated with damage to subcortical language pathways. Underlying mechanisms still need to be better understood, complicating preoperative risk assessment. This study compared qualitative and quantitative functionally relevant subcortical differences pre- and directly postoperatively in glioma patients with and without aphasia.

Methods: Language-relevant cortical sites were defined using navigated transcranial magnetic stimulation (nTMS) language mapping in 74 patients between 07/2016 and 07/2019. Post-hoc nTMS-based diffusion tensor imaging tractography was used to compare a tract's pre- and postoperative visualization, volume and fractional anisotropy (FA), and the preoperative distance between tract and lesion and postoperative overlap with the resection cavity between the following groups: no aphasia (NoA), tumor- or previous resection induced aphasia persistent pre- and postoperatively (TIA_P), and surgery-induced transient or permanent aphasia (SIA_T or SIA_P).

Results: Patients with NoA, TIA_P, SIA_T, and SIA_P showed distinct fasciculus arcuatus (AF) and inferior-fronto-occipital fasciculus (IFOF) properties. The AF was more frequently reconstructable, and the FA of IFOF was higher in NoA than TIA_P cases (all p ≤ 0.03). Simultaneously, SIA_T cases showed higher IFOF fractional anisotropy than TIA_P cases (p < 0.001) and the most considerable AF volume loss overall. While not statistically significant, the four SIA_P cases showed complete loss of ventral language streams postoperatively, the highest resection-cavity-AF-overlap, and the shortest AF to tumor distance.

Conclusion: Functionally relevant qualitative and quantitative differences in AF and IFOF provide a pre- and postoperative pathophysiological and clinically relevant diagnostic indicator that supports surgical risk stratification.

Citing Articles

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PMID: 39551912 PMC: 11611971. DOI: 10.1007/s00429-024-02859-4.

References

Sarubbo S, Tate M, De Benedictis A, Merler S, Moritz-Gasser S, Herbet G . Mapping critical cortical hubs and white matter pathways by direct electrical stimulation: an original functional atlas of the human brain. Neuroimage. 2019; 205:116237. PMC: 7217287. DOI: 10.1016/j.neuroimage.2019.116237. View

Ille S, Engel L, Kelm A, Meyer B, Krieg S . Language-Eloquent White Matter Pathway Tractography and the Course of Language Function in Glioma Patients. Front Oncol. 2018; 8:572. PMC: 6291459. DOI: 10.3389/fonc.2018.00572. View

Catani M, Thiebaut de Schotten M, Slater D, DellAcqua F . Connectomic approaches before the connectome. Neuroimage. 2013; 80:2-13. DOI: 10.1016/j.neuroimage.2013.05.109. View

Sarubbo S, De Benedictis A, Maldonado I, Basso G, Duffau H . Frontal terminations for the inferior fronto-occipital fascicle: anatomical dissection, DTI study and functional considerations on a multi-component bundle. Brain Struct Funct. 2011; 218(1):21-37. DOI: 10.1007/s00429-011-0372-3. View

Mandonnet E, Nouet A, Gatignol P, Capelle L, Duffau H . Does the left inferior longitudinal fasciculus play a role in language? A brain stimulation study. Brain. 2007; 130(Pt 3):623-9. DOI: 10.1093/brain/awl361. View

Picht T, Krieg S, Sollmann N, Rosler J, Niraula B, Neuvonen T . A comparison of language mapping by preoperative navigated transcranial magnetic stimulation and direct cortical stimulation during awake surgery. Neurosurgery. 2013; 72(5):808-19. DOI: 10.1227/NEU.0b013e3182889e01. View

Duffau H, Moritz-Gasser S, Mandonnet E . A re-examination of neural basis of language processing: proposal of a dynamic hodotopical model from data provided by brain stimulation mapping during picture naming. Brain Lang. 2013; 131:1-10. DOI: 10.1016/j.bandl.2013.05.011. View

Lioumis P, Zhdanov A, Makela N, Lehtinen H, Wilenius J, Neuvonen T . A novel approach for documenting naming errors induced by navigated transcranial magnetic stimulation. J Neurosci Methods. 2011; 204(2):349-54. DOI: 10.1016/j.jneumeth.2011.11.003. View

Fekonja L, Wang Z, Bahrend I, Rosenstock T, Rosler J, Wallmeroth L . Manual for clinical language tractography. Acta Neurochir (Wien). 2019; 161(6):1125-1137. PMC: 6525736. DOI: 10.1007/s00701-019-03899-0. View

10.

Li Y, Guo J, Zhang K, Wei H, Fan J, Yu S . Diffusion tensor imaging versus intraoperative subcortical mapping for glioma resection: a systematic review and meta-analysis. Neurosurg Rev. 2023; 46(1):154. PMC: 10307847. DOI: 10.1007/s10143-023-02058-5. View

11.

Latini F, Martensson J, Larsson E, Fredrikson M, Ahs F, Hjortberg M . Segmentation of the inferior longitudinal fasciculus in the human brain: A white matter dissection and diffusion tensor tractography study. Brain Res. 2017; 1675:102-115. DOI: 10.1016/j.brainres.2017.09.005. View

12.

Le Bihan D, Poupon C, Amadon A, Lethimonnier F . Artifacts and pitfalls in diffusion MRI. J Magn Reson Imaging. 2006; 24(3):478-88. DOI: 10.1002/jmri.20683. View

13.

Ivanova M, Isaev D, Dragoy O, Akinina Y, Petrushevskiy A, Fedina O . Diffusion-tensor imaging of major white matter tracts and their role in language processing in aphasia. Cortex. 2016; 85:165-181. DOI: 10.1016/j.cortex.2016.04.019. View

14.

Raffa G, Marzano G, Curcio A, Espahbodinea S, Germano A, Angileri F . Personalized surgery of brain tumors in language areas: the role of preoperative brain mapping in patients not eligible for awake surgery. Neurosurg Focus. 2024; 53(6):E3. DOI: 10.3171/2022.9.FOCUS22415. View

15.

Poologaindran A, Profyris C, Young I, Dadario N, Ahsan S, Chendeb K . Interventional neurorehabilitation for promoting functional recovery post-craniotomy: a proof-of-concept. Sci Rep. 2022; 12(1):3039. PMC: 8866464. DOI: 10.1038/s41598-022-06766-8. View

16.

Catani M, Jones D, Donato R, Ffytche D . Occipito-temporal connections in the human brain. Brain. 2003; 126(Pt 9):2093-107. DOI: 10.1093/brain/awg203. View

17.

Duffau H, Herbet G, Moritz-Gasser S . Toward a pluri-component, multimodal, and dynamic organization of the ventral semantic stream in humans: lessons from stimulation mapping in awake patients. Front Syst Neurosci. 2013; 7:44. PMC: 3752437. DOI: 10.3389/fnsys.2013.00044. View

18.

Awiszus F . TMS and threshold hunting. Suppl Clin Neurophysiol. 2003; 56:13-23. DOI: 10.1016/s1567-424x(09)70205-3. View

19.

Southwell D, Riva M, Jordan K, Caverzasi E, Li J, Perry D . Language outcomes after resection of dominant inferior parietal lobule gliomas. J Neurosurg. 2017; 127(4):781-789. DOI: 10.3171/2016.8.JNS16443. View

20.

Krishna S, Kakaizada S, Almeida N, Brang D, Hervey-Jumper S . Central Nervous System Plasticity Influences Language and Cognitive Recovery in Adult Glioma. Neurosurgery. 2021; 89(4):539-548. PMC: 8440067. DOI: 10.1093/neuros/nyaa456. View