A taxonomy for cerebellar cavernous malformations: subtypes of cerebellar lesions.

OBJECTIVE: An anatomical taxonomy has been established to guide surgical approach selection for resecting brainstem and deep and superficial cerebral cavernous malformations (CMs). The authors propose a novel taxonomy for cerebellar CMs, introduce 6 distinct neuroanatomical subtypes, and assess their clinical outcomes. METHODS: This bi-institutional, 2-surgeon cohort study included 143 cerebellar CMs that were microsurgically treated over a 25-year period. The proposed taxonomy classifies cerebellar CMs into 6 subtypes on the basis of anatomical location as identified on preoperative MR imaging. Neurological outcomes were assessed using the modified Rankin Scale (mRS), and outcomes were compared among the subtypes, with favorable outcomes defined as mRS scores ≤ 2. RESULTS: A total of 143 cerebellar CMs were resected in 140 patients. The mean (SD) age was 42.3 (15.2) years; 86 (60%) of the cerebellar CMs were in women, and 57 (40%) were in men. Cerebellar subtypes were suboccipital (17%, 25/143); tentorial (9%, 13/143); petrosal (43%, 62/143); vermian (13%, 18/143); tonsillar (2%, 3/143); and deep nuclear (15%, 22/143). Overall, 78 of 143 (55%) cerebellar CMs presenting to a cerebellar surface were resected without tissue transgression, and the remaining CMs (65/143, 45%) required translobular or transsulcal approaches. Complete resection was achieved in 134 of 143 cases (94%). Favorable outcomes were achieved in 91% (129/141) of cases with follow-up at a mean (SD) follow-up duration of 37.4 (53.8) months. Relative outcomes were unchanged or improved relative to the preoperative baseline in 93% (131/141) of cases with follow-up, without differences between subtypes. CONCLUSIONS: Most cerebellar CMs are convexity lesions that do not require deep dissection. However, transsulcal and fissural approaches are used for those beneath the cerebellar surface to minimize tissue transgression and preserve associated function. Complete resection without any new deficit is accomplished in most patients. The proposed taxonomy for cerebellar CMs (suboccipital, tentorial, petrosal, vermian, tonsillar, and deep nuclear) guides the selection of craniotomy and approach to enhance patient safety and optimize neurological outcomes.

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

OBJECTIVE: 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. METHODS: 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. RESULTS: 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). CONCLUSIONS: 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.

A taxonomy for superficial cerebral cavernous malformations: subtypes of cortical and subcortical lesions.

OBJECTIVE: A taxonomy for superficial cerebral cavernous malformations (CMs), those based cortically in gyral gray matter or subcortically in underlying white matter, is proposed to build on the comprehensive, systematic characterization of CMs in the entire brain. METHODS: Patients with superficial cerebral CMs were retrospectively analyzed from a consecutive surgical series between November 2008 and June 2021 at the authors' center. Superficial cerebral CMs were categorized into 4 subtypes based on their cortical location or, if subcortical, proximity to the nearest cerebral surface: convexity, medial, basal, and sylvian. Lobar location was also included for subtyping: frontal, temporal, parietal, and occipital. RESULTS: A total of 362 CMs were resected in 346 patients. CM subtypes were as follows: 132 (36.5%) convexity, 78 (21.5%) medial, 72 (19.9%) basal, and 80 (22.1%) sylvian. Frontal CMs were most common (155 [42.8%]), followed by parietal (89 [24.6%]), temporal (87 [24.0%]), and occipital (31 [8.6%]). Of all CMs, 302 (83.4%) were cortical and 60 (16.6%) were subcortical. The mean subcortical depth of deep lesions was 2.97 cm, and the mean lesion volume was 4.68 cm3. Overall, 228 lesions (63.0%) were resected through a transgyral approach, and 134 (37.0%) were resected through a transsulcal approach. Good outcomes (modified Rankin Scale [mRS] score ≤ 2) were observed in 314 patients (86.7%) and poor outcomes (mRS score > 2) in 25 patients (6.9%), and 23 patients (6.4%) were lost to late follow-up (mean follow-up duration 11.5 months). Relative outcomes were good (unchanged or improved mRS score) in 327 patients (90.3%) and poor (worse or died) in 35 patients (9.7%). CONCLUSIONS: Superficial cerebral CMs were resected through a gyrus or sulcus to open the subarachnoid dissection corridors, traversing the full extent of sulci to deepen the approach and minimize tissue transgression. Transgyral dissection avoids associated arteries but is inherently transgressive, whereas transsulcal dissection preserves cortical tissue and may reduce morbidity. Superficial cerebral CMs occupy the largest territory of the 7 types, and the size and surface complexity of the cerebrum make taxonomic subtyping valuable for clear anatomical description.