Neuropsychological outcomes after pediatric epilepsy surgery: Role of electrical stimulation language mapping

Abstract

We studied the association between electrical stimulation mapping (ESM) with a visual naming task and post-operative neuropsychological outcomes after pediatric epilepsy surgery. Methods: Children who underwent epilepsy surgery, having pre-and 1-year post-surgery neuropsychological evaluation (NPE) available, were included. NPE scores were transformed using principal components (PC) analysis. The relationship between post-surgical PC scores, adjusted for pre-surgery PC scores, and ESM was analyzed. Clinical variables influencing this relationship were also sought. Results: One hundred and four children (89 patients > 5 years-old, and 15 patients 3−5 years-old) were included. Among children > 5 years-of-age, a significant effect of language ESM was observed on all 3 post-surgery PC scores adjusted for respective pre-surgery PC scores. Specifically, only 30 % patients who underwent language ESM had a decrease in PC1 scores ≥1-year after epilepsy surgery, compared to 68 % those who did not undergo language ESM (p = 0.001). Seizure outcomes, age at the time of surgery, predominant seizure type, and family history of epilepsy were other significant determinants of post-surgical PC scores including a change in PC scores from pre-surgery baseline. Combinations of pre-surgical variables were able to predict post-surgical PC scores with high specificity. In children aged 3−5 years, no significant effect of language ESM was seen on postsurgery PC scores adjusted for respective pre-surgery PC scores. Conclusions: Speech/language ESM should be performed more widely in patients > 5 years-of-age undergoing epilepsy surgery. Also, more efficient brain mapping techniques and language paradigms are needed for younger children.

Electrical Stimulation Mapping of Brain Function: A Comparison of Subdural Electrodes and Stereo-EEG

“…ESM can also help anticipate and prepare for post-operative deficits if there is an overlap between the seizure-onset zone and eloquent functional regions. With SDE, although earlier studies were somewhat discordant (Lendt et al, 1999;de Koning et al, 2009;Skirrow et al, 2011;Puka et al, 2017), a recent large study has demonstrated the relationship between ESM and neuropsychological outcomes (Sakpichaisakul et al, 2020). A multi-center study with sufficient sample size, using valid and comprehensive age-appropriate assessments, both pre-and post-operatively, to establish the predictive value of SEEG ESM for neurological outcomes is imminently needed.…”

“…While epilepsy surgery can improve executive function and memory in some patients, probably by removing the pathological effects of seizures and epileptiform discharges, more frequently it is associated with a decline in verbal memory, naming, attention, and other domains (Lendt et al, 1999;de Koning et al, 2009;Ives-Deliperi and Butler, 2012). The neuropsychological outcomes after epilepsy surgery are driven by multiple factors, including but not limited to the age at onset of seizures, age at the time of surgery, anti-seizure medications, presence and nature of an epileptogenic lesion, location of the seizure-onset zone, its relationship with the eloquent cortices, neurosurgical planning, and most importantly, post-operative seizure outcomes (Skirrow et al, 2011;Puka et al, 2017;Sakpichaisakul et al, 2020). Whether pre-surgical ESM reduces the risk of adverse postoperative outcomes, over and above what may be expected from demographic and clinical information, remains a vexing question.…”

“…Significantly worse post-operative language function after dominant anterior temporal lobectomy (ATL) was reported in 13/15 patients in one study (Hermann and Wyler, 1988), while no significant deterioration in neuropsychological scores were reported in 18 patients after dominant ATL in another study (Davies et al, 1994). Recently, in 89 patients aged 6-24 years, comprehensive standardized pre-and 1-year post-operative neuropsychological data were examined to evaluate the impact of pre-surgical ESM with SDE (Sakpichaisakul et al, 2020). The multi-domain neuropsychological data were collapsed into three principal component scores representing general cognition, memory, and naming.…”

“…Only 30% of patients who underwent language ESM experienced a postoperative decrease in general cognition score, compared to 68% of those who did not. Whereas the above study used only a visual naming task for language ESM that is often considered the gold-standard (Hamberger, 2007;Sakpichaisakul et al, 2020), others have emphasized the need for including multiple languages tasks (Wellmer et al, 2009). In a study where language ESM was performed extra-operatively in 12 patients, and intra-operatively in seven patients, all undergoing dominant temporal lobe surgery, all visual naming sites were preserved (Hamberger et al, 2005).…”

“…Also, it may be desirable to routinely evaluate for interference with voluntary movements during ESM, to map for ''negative'' motor areas, which may require higher current strengths and sustained patient participation (Kanno et al, 2018). Studies with SDE have shown that neuropsychological deficits do occur after epilepsy surgeries guided by language ESM, particularly in higher-order cognitive domains which may underlie linguistic development and ability, but may not be crucial for cued naming, thus demonstrating the need for multi-paradigm ESM to evaluate different domains (Wellmer et al, 2009;Sakpichaisakul et al, 2020). Although assessment of positive motor responses and patient-reported sensory responses is fairly straightforward, the sensitivity of sensorimotor ESM may be further refined by the use of surface electromyography to detect visually obscure muscle contractions, and by evaluation for negative motor responses by white matter stimulation (Rech et al, 2016(Rech et al, , 2017.…”