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Eloquent noneloquence: redefinition of cortical eloquence based on outcomes of superficial cerebral cavernous malformation resection
Journal article   Peer reviewed

Eloquent noneloquence: redefinition of cortical eloquence based on outcomes of superficial cerebral cavernous malformation resection

Benjamin K Hendricks, Lea Scherschinski, Jubran H Jubran, Nicholas B Dadario, Katherine Karahalios, Dimitri Benner, Danielle VanBrabant and Michael T Lawton
Journal of neurosurgery, Vol.141(2), pp.291-305
08/01/2024
PMID: 38457787

Abstract

Adolescent Adult Aged Cerebral Cortex - diagnostic imaging Cerebral Cortex - surgery Female Hemangioma, Cavernous, Central Nervous System - surgery Humans Magnetic Resonance Imaging Male Microsurgery - methods Middle Aged Neurosurgical Procedures - methods Retrospective Studies Treatment Outcome Young Adult
Cerebral cavernous malformations (CMs) are pathological lesions that cause discrete cortical disruption with hemorrhage, and their transcortical resections can cause additional iatrogenic disruption. The analysis of microsurgically treated CMs might identify areas of "eloquent noneloquence," or cortex that is associated with unexpected deficits when injured or transgressed. Patients from a consecutive microsurgical series of superficial cerebral CMs who presented to the authors' center over a 13-year period were retrospectively analyzed. Neurological outcomes were measured using the modified Rankin Scale (mRS), and new, permanent neurological or cognitive symptoms not detected by changes in mRS scores were measured as additional functional decline. Patients with multiple lesions and surgical encounters for different lesions within the study interval were represented within the cohort as multiple patient entries. Virtual object models for CMs and approach trajectories to subcortical lesions were merged into a template brain model for subtyping and Quicktome connectomic analyses. Parcellation outputs from the models were analyzed for regional cerebral clustering. Overall, 362 CMs were resected in 346 patients, and convexity subtypes were the most common (132/362, 36.5%). Relative to the preoperative mRS score, 327 of 362 cases (90.3%) were in patients who improved or remained stable, 35 (9.7%) were in patients whose conditions worsened, and 47 (13.0%) were in patients who had additional functional decline. Machine learning analyses of lesion objects and trajectory cylinder mapping identified 7 hotspots of novel eloquence: supplementary motor area (bilateral), anterior cingulate cortex (bilateral), posterior cingulate cortex (bilateral), anterior insula (left), frontal pole (right), mesial temporal lobe (left), and occipital cortex (right). Transgyral and transsulcal resections that circumvent areas of traditional eloquence and navigate areas of presumed noneloquence may nonetheless result in unfavorable outcomes, demonstrating that brain long considered by neurosurgeons to be noneloquent may be eloquent. Eloquent hotspots within multiple large-scale networks redefine the neurosurgical concept of eloquence and call for more refined dissection techniques that maximize transsulcal dissection, intracapsular resection, and tissue preservation. Human connectomics, awareness of brain networks, and prioritization of cognitive outcomes require that we update our concept of cortical eloquence and incorporate this information into our surgical strategies.

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