Supplementary Motor Area Resection Research Articles

Child Neurology: Neurophysiologic and Anatomical Correlates in Startle Epilepsy: A Comprehensive SEEG Investigation for Successful Resective Surgery.

Startle epilepsy, characterized by startle-provoked epileptic seizures, was historically recognized as one of the reflex epilepsies but currently lacks classification as a specific epileptic syndrome because of insufficient characterization. This study presents an institutional experience and review of relevant literature focusing on the neurophysiologic and anatomical aspects of startle epilepsy. We describe a pediatric patient with an underlying structural etiology of left frontal encephalomalacia who continued to experience disabling seizures despite multiple antiseizure medications and previous palliative surgery. A comprehensive presurgical evaluation using SEEG led to the resection of the left supplementary motor area and adjacent middle cingulate cortex, resulting in successful seizure remission. A literature review on the surgical treatment of startle epilepsy revealed consistent reports of successful seizure remission through neocortical resection of the supplementary motor area and/or cingulate region. This case study and literature review highlights startle epilepsy as a distinct form of epilepsy with identifiable neurophysiologic and anatomical characteristics. Our observations emphasize the potential of resective surgery as a viable treatment option for startle epilepsy and underscore the importance of neurophysiologic monitoring in guiding surgical interventions.

Resection of supplementary motor area gliomas: revisiting supplementary motor syndrome and the role of the frontal aslant tract.

The supplementary motor area (SMA) is an eloquent region that is frequently a site for glioma, or the region is included in the resection trajectory to deeper lesions. Although the clinical relevance of SMA syndrome has been well described, it is still difficult to predict who will become symptomatic. The object of this study was to define which patients with SMA gliomas would go on to develop a postoperative SMA syndrome. The University of California, San Francisco, tumor registry was searched for patients who, between 2010 and 2019, had undergone resection for newly diagnosed supratentorial diffuse glioma (WHO grades II-IV) performed by the senior author and who had at least 3 months of follow-up. Pre- and postoperative MRI studies were reviewed to confirm the tumor was located in the SMA region, and the extent of SMA resection was determined by volumetric assessment. Patient, tumor, and outcome data were collected retrospectively from documents available in the electronic medical record. Tumors were registered to a standard brain atlas to create a frequency heatmap of tumor volumes and resection cavities. During the study period, 56 patients (64.3% male, 35.7% female) underwent resection of a newly diagnosed glioma in the SMA region. Postoperatively, 60.7% developed an SMA syndrome. Although the volume of tumor within the SMA region did not correlate with the development of SMA syndrome, patients with the syndrome had larger resection cavities in the SMA region (25.4% vs 14.2% SMA resection, p = 0.039). The size of the resection cavity in the SMA region did not correlate with the severity of the SMA syndrome. Patients who developed the syndrome had cavities that were located more posteriorly in the SMA region and in the cingulate gyrus. When the frontal aslant tract (FAT) was preserved, 50% of patients developed the SMA syndrome postoperatively, whereas 100% of the patients with disruption of the FAT during surgery developed the SMA syndrome (p = 0.06). Patients with SMA syndrome had longer lengths of stay (5.6 vs 4.1 days, p = 0.027) and were more likely to be discharged to a rehabilitation facility (41.9% vs 0%, p < 0.001). There was no difference in overall survival for newly diagnosed glioblastoma patients with SMA syndrome compared to those without SMA syndrome (1.6 vs 3.0 years, p = 0.33). For patients with SMA glioma, more extensive resections and resections involving the posterior SMA region and posterior cingulate gyrus increased the likelihood of a postoperative SMA syndrome. Although SMA syndrome occurred in all cases in which the FAT was resected, FAT preservation does not reliably avoid SMA syndrome postoperatively.

Recovery time from supplementary motor area syndrome: relationship to postoperative day 7 paralysis and damage of the cingulum.

Supplementary motor area (SMA) syndrome is defined as temporary paralysis after the resection of brain tumor localized in the SMA. Although in most cases paralysis induced by SMA resection resolves within a short period, the time until complete recovery varies and has not been precisely analyzed to date. In this study, the authors investigated factors for predicting the time required for recovery from paralysis after SMA resection. Data from 20 cases were analyzed. All 20 patients (mean age 54.9 ± 12.6 years) had undergone resection of frontal lobe glioma involving the SMA. The severity of postoperative paralysis was recorded until complete recovery using the Brunnstrom recovery stage index. To investigate factors associated with recovery time, the authors performed multivariate analysis with the following potentially explanatory variables: age, severity of paralysis after the surgery, resected volume of the SMA, and probability of disconnection of fibers running through or near the SMA. Moreover, voxel-based lesion symptom analysis was performed to clarify the resected regions related to prolonged recovery. In most cases of severe to moderate paralysis, there was substantial improvement within the 1st postoperative week, but 2-9 weeks were required for complete recovery. Significantly delayed recovery from paralysis was associated with resection of the cingulate cortex and its deep regions. The factors found to influence recovery time from paralysis were stage of paralysis at postoperative day 7 and disconnection probability of the cingulum (adjusted R2 = 0.63, p < 0.0001). Recovery time from paralysis due to SMA syndrome can be predicted by the severity of paralysis at postoperative day 7 and degree of damage to the cingulum.

F192. Role of multimodal extra and intraoperative Stereoelectroencephalography (sEEG) monitoring in tailoring staged surgical resection in patients with eloquent cortex (Rolandic) pharmacoresistant epilepsy

Introduction To describe the feasibility, safety and seizure outcome of patients with medically intractable rolandic epilepsy(RE) who underwent staged resections guided by multimodal extra and intraoperative SEEG recordings. Methods We retrospectively studied and analyzed patients, who underwent extra and intraoperative intracranial invasive stereoEEG monitoring, data related to semiology, non-invasive electrophysiology, imaging, type of resection, complications, surgical pathology results and seizure outcome from January 2015 through September 2017, under Cleveland Clinic IRB. Results Five patients were identified as having intractable RE based on analysis of pre-surgical evaluation using 3T magnetic resonance imaging (MRI), magnetoencephalography(MEG) and positron emission tomography (PET). Preoperative magnetic resonance imaging were considered nonlesional in all five patients but after the pre-surgical evaluation, there were abnormal sulcation pattern or increased signal in white matter were noticed which are of unknown significance. All five patients were underwent sEEG implantation with hypothesis of peri-rolandic or paracentral lobule regions being epileptogenic. Extra-operative sEEG data in all patients showed ictal onset zone involving rolandic cortex (hand knob and paracentral lobule), premotor and/or supplementary motor area (SMA). In two patients, hand knob rolandic cortex was the region of interest The other three being paracentral lobule (leg motor). Given all the data (semiology, sEEG data and pre-sugical evaluation), the conclusion of epileptogenic zone (EZ) being close proximity to eloquent cortex. Given the semiology, staged resection approach with continuous sEEG recording was performed in the operating room. Resection of interictally active non-eloquent cortex electrodes was performed first guided by real-time intraoperative sEEG (electrophysiology) data. The resection was also guided by the sEEG electrode in three dimensions. Resolution of rolandic hand motor spike activities was documented after resection of SMA in three patients, cingulate and pre-motor areas in one patient. In the last patient, hand sensory area was resected sparing motor cortex. Three out of five patients did not have any deficit but two had mild foot drop. Pathology showed focal cortical dysplasia type (IB, IIA, and IIB) and a possible vascular malformation in another. All patients were reported to be seizure free at follow up period of 6–28 months. Conclusion Taken into account of hyper-synchronous connectivity in frontal and parietal rolandic regions, we present a case series of patients who underwent staged resections guided by a novel multimodal method of invasive monitoring. The results of this highly selected group of patients testify for the feasibility and safety of a novel multimodal method of invasive monitoring, combining the benefits of both intra and extra-operative SEEG recording, especially operating around the central lobule near hand knob regions.

Neuropsychological outcome following frontal lobectomy for pharmacoresistant epilepsy in adults.

This retrospective cohort study characterized cognitive and motor outcomes in a large sample of adults who underwent frontal lobe resections for treatment of pharmacoresistant epilepsy. Ninety patients who underwent unilateral frontal lobe resection for epilepsy (42 language-dominant hemisphere/48 nondominant hemisphere) between 1989 and 2014 completed comprehensive preoperative and postoperative neuropsychological evaluations that included measures of verbal and nonverbal intellectual functioning, attention/working memory, processing speed, language, executive functioning, verbal and visual memory, and motor functioning. Objective methods were used to assess meaningful change across a wide range of abilities and to identify factors associated with neuropsychological decline following frontal lobectomy. Detailed postoperative neuroimaging analysis was conducted to characterize region, extent, and volume of resection. Forty-eight percent of patients did not demonstrate meaningful postoperative declines in cognition and an additional 42% demonstrated decline in 1 or 2 cognitive domains. When cognitive decline was observed, it usually occurred on measures of intelligence, visuomotor processing speed, or executive functioning. Side and site of resection were unrelated to cognitive outcome, but played a role in decline of contralateral manual dexterity following supplementary motor area resection. Higher preoperative ability, older age at surgery, absence of a malformation of cortical development on MRI, and poor seizure outcome were related to cognitive decline on some measures, but had poor sensitivity in identifying at-risk patients. The vast majority of patients who undergo frontal lobectomy for treatment of pharmacoresistant epilepsy demonstrate good cognitive and motor outcomes.

Risk factor analysis of the development of new neurological deficits following supplementary motor area resection

Supplementary motor area (SMA) resection often induces postoperative contralateral hemiparesis or speech disturbance. This study was performed to assess the neurological impairments that often follow SMA resection and to assess the risk factors associated with these postoperative deficits. The records for patients who had undergone SMA resection for pharmacologically intractable epilepsy between 1994 and 2010 were gleaned from an epilepsy surgery database and retrospectively reviewed in this study. Forty-three patients with pharmacologically intractable epilepsy underwent SMA resection with intraoperative cortical stimulation and mapping while under awake anesthesia. The mean patient age was 31.7 years (range 15-63 years), and the mean duration and frequency of seizures were 10.4 years (range 0.1-30 years) and 14.6 per month (range 0.1-150 per month), respectively. Pathological examination of the brain revealed cortical dysplasia in 18 patients (41.9%), tumors in 16 patients (37.2%), and other lesions in 9 patients (20.9%). The mean duration of the follow-up period was 84.0 months (range 24-169 months). After SMA resection, 23 patients (53.5%) experienced neurological deficits. Three patients (7.0%) experienced permanent deficits, and 20 (46.5%) experienced symptoms that were transient. All permanent deficits involved contralateral weakness, whereas the transient symptoms patients experienced were varied, including contralateral weaknesses in 15, apraxia in 1, sensory disturbances in 1, and dysphasia in 6. Thirteen patients recovered completely within 1 month. Univariate analysis revealed that resection of the SMA proper, a shorter lifetime seizure history (<10 years), and resection of the cingulate gyrus in addition to the SMA were associated with the development of neurological deficits (p=0.078, 0.069, and 0.023, respectively). Cingulate gyrus resection was the only risk factor identified on multivariate analysis (p=0.027, OR 6.530, 95% CI 1.234-34.562). Resection of the cingulate gyrus in addition to the SMA was significantly associated with the development of postoperative neurological impairment.

Persistent verbal and behavioral deficits after resection of the left supplementary motor area in epilepsy surgery

An 8-year-old boy underwent a resection for focal cortical dysplasia at the left supplementary motor area (SMA) for the treatment of intractable epilepsy. The manifestations of SMA syndrome, such as transient mutism and right hemiparesis, resolved within a few weeks. Verbal disfluency and impaired executive function, accompanied by impulsivity and distractibility, persisted for more than 12months. The verbal and behavioral problems caused serious difficulties in the school life of the patient, until they became less evident at 18months after surgery. Tractography performed 18months after surgery revealed a defect in the subportion of fronto-parietal association fibers within the left superior longitudinal fascicles. Verbal influency can persist with unusually long duration after resection of SMA during childhood. Although not discernible on the routine neuroimaging, white matter damage beneath the SMA region could result in serious disabilities in executive function. These complications should be recognized for the prediction and assessment of deficits in children after surgical intervention involving this region.

Assessment of morbidity following resection of cingulate gyrus gliomas

The morbidity associated with resection of tumors in the cingulate gyrus (CG) is not well established. The goal of the present study is to define the short- and long-term morbidity profile associated with resection of gliomas within this region. Ninety consecutive patients with gliomas involving the CG were analyzed. Resections were classified by zones corresponding to functionally defined regions of the CG as follows: Zone I (perigenual, anterior), Zone II (midcingulate), Zone III (posterior), and Zone IV (retrosplenial). Basic demographic, imaging, operative details, and pre- and postoperative neurological examinations were recorded for each patient. Patients in whom neurological morbidity was documented during their initial postoperative examination who did not completely improve by the 6-month follow-up examination were considered to have a permanent deficit. For each patient with surgery-related morbidity, postoperative MR imaging and operative notes were reviewed, and the cortical regions incorporated in the surgical trajectory were recorded. The analysis was carried out for tumors confined to the CG (> 90% of tumor contained within the CG) as well as those involving the CG but extending into adjacent cortical structures. Analysis of the entire patient cohort demonstrated that 29% of patients experienced a new or worsened neurological deficit immediately after surgery. The most common deficits were supplementary motor area (SMA) syndrome (20%), weakness (6%), and sensory changes (2%). All patients with an SMA syndrome in our series had intentional resection of SMA as part of the surgical approach. Patients with resections including Zone II or III had a higher rate of total morbidity and SMA syndrome than patients with Zone I resections (p < 0.05). Only 4% of patients had a persistent neurological deficit at 6 months postoperatively. A similar morbidity profile was observed in the subset analysis of patients with tumors confined to the CG, with no additional morbidity related to known cingulate-specific functions. Resection of gliomas involving the CG can be performed with minimal, predictable long-term morbidity (< 5%). Surgical morbidity is primarily a function of surgical trajectory rather than the particular cingulate region resected.

Outcome of epilepsy surgery in patients investigated with subdural electrodes

Invasive intracranial electrodes (IE) are an important part of the work-up in many patients being considered for epilepsy surgery. Because IE are usually reserved for cases where seizure localization is ambiguous, one might expect that the eventual outcome of epilepsy surgery in these patients would be worse than in patients who did not require IE as part of their work-up. The purpose of this study was to specifically examine those patients who underwent insertion of subdural electrodes, to determine how many of these patients eventually underwent resective surgery of any type and to assess the eventual outcome. All cases admitted for subdural electrodes between January 2000 and June 2005 were reviewed. Surgical outcomes were reported using the Engel classification and a multivariate analysis was used to determine which factors were associated with successful surgery. 177 IE implantations were performed in 172 patients. Of these, 130 patients went on to have surgery. In the 113 of the 130 surgical patients in whom 1-year follow-up was available, 47% were seizure free at 1 year. Age was a major predictor of outcome with only 21% of patients over age 40 becoming seizure free with surgery compared to 58% in patients aged under 40 years (p=0.0004). Other predictors of an Engel I outcome included having a temporal lobectomy or supplementary motor area resection. Good results from eventual resective surgery can be achieved in patients needing invasive recordings. Younger patients with temporal lobe epilepsy seem to have the highest likelihood of seizure freedom.

INCIDENCE AND CLINICAL EVOLUTION OF POSTOPERATIVE DEFICITS AFTER VOLUMETRIC STEREOTACTIC RESECTION OF GLIAL NEOPLASMS INVOLVING THE SUPPLEMENTARY MOTOR AREA

We report the incidence and clinical evolution of postoperative deficits and supplementary motor area (SMA) syndrome after volumetric stereotactic resection of glial neoplasms involving the posterior one-third of the superior frontal convolution. We investigated variables that may be associated with the occurrence of SMA syndrome. The postoperative clinical status of 27 consecutive patients who underwent resection of SMA gliomas was retrospectively reviewed. Neurological examination results were recorded 1 day, 1 week, 1 month, and 6 months postoperatively. The extent of tumor resection, the percentage of SMA resection, violation of the cingulate gyrus, and operative complications were tabulated. The overall incidence of SMA-related deficits was 26% (7 of 27 patients), with 3 patients having complete SMA syndrome and 4 patients having partial SMA syndrome. Two additional patients (7.5%) had other postoperative deficits, including one with mild facial weakness and one with transient aphasia. The resection of low-grade gliomas was associated with a higher incidence of SMA syndrome, an outcome that likely reflects more complete removal of functional SMA cortex in this subset of patients. Intraoperative monitoring localized the precentral sulcus within the preoperatively defined tumor volume in 6 (22%) of 27 patients, thereby precluding gross total resection. All 27 patients had excellent outcomes at the 6-month follow-up examination. When the resection of SMA gliomas is limited to the radiographic tumor boundaries, the incidence and severity of SMA syndrome may be minimized. With the use of these resection parameters, patients with high-grade SMA gliomas are unlikely to experience SMA syndrome. These findings are helpful in the preoperative counseling of patients who are to undergo cytoreductive resection of SMA gliomas.

Role of the healthy hemisphere in recovery after resection of the supplementary motor area

To determine the compensatory mechanisms involved in the recovery of motor function following surgical lesions of the supplementary motor area (SMA) and their relation to the clinical characteristics of recovery. Twelve patients were referred for surgery of low-grade gliomas located in the SMA, and compared to eight healthy controls using fMRI before and after surgery during self-paced movements of both hands, successively. Magnitude and volume of activation within regions of interest (primary sensorimotor cortex, premotor cortex, SMA, preSMA, and parietal lobes) were compared and tested for correlation with anatomic characteristics of the tumor and resection, and clinical data. Tumor growth induced preoperative underactivity in the adjacent SMA and overactivity in the opposite SMA. Postoperative recovery was associated with recruitment of a premotor network located in the healthy hemisphere including the SMA and the lateral premotor cortex. Postoperative premotor recruitment in the healthy hemisphere increased with the percentage of resection of preoperative SMA activation. Shortened onset and duration of recovery was associated with increased preoperative changes in activation levels. These findings suggest a dysfunction of the SMA ipsilateral to the tumor, partially compensated by a recruitment of the contralesional SMA which correlated with shortened postoperative recovery. SMA resection was compensated by the recruitment of a medial and lateral premotor circuitry in the healthy hemisphere.

Incidence and clinical evolution of postoperative deficits after volumetric stereotactic resection of glial neoplasms involving the supplementary motor area.

We report the incidence and clinical evolution of postoperative deficits and supplementary motor area (SMA) syndrome after volumetric stereotactic resection of glial neoplasms involving the posterior one-third of the superior frontal convolution. We investigated variables that may be associated with the occurrence of SMA syndrome. The postoperative clinical status of 27 consecutive patients who underwent resection of SMA gliomas was retrospectively reviewed. Neurological examination results were recorded 1 day, 1 week, 1 month, and 6 months postoperatively. The extent of tumor resection, the percentage of SMA resection, violation of the cingulate gyrus, and operative complications were tabulated. The overall incidence of SMA-related deficits was 26% (7 of 27 patients), with 3 patients having complete SMA syndrome and 4 patients having partial SMA syndrome. Two additional patients (7.5%) had other postoperative deficits, including one with mild facial weakness and one with transient aphasia. The resection of low-grade gliomas was associated with a higher incidence of SMA syndrome, an outcome that likely reflects more complete removal of functional SMA cortex in this subset of patients. Intraoperative monitoring localized the precentral sulcus within the preoperatively defined tumor volume in 6 (22%) of 27 patients, thereby precluding gross total resection. All 27 patients had excellent outcomes at the 6-month follow-up examination. When the resection of SMA gliomas is limited to the radiographic tumor boundaries, the incidence and severity of SMA syndrome may be minimized. With the use of these resection parameters, patients with high-grade SMA gliomas are unlikely to experience SMA syndrome. These findings are helpful in the preoperative counseling of patients who are to undergo cytoreductive resection of SMA gliomas.

“Supplementary motor area (SMA) seizure” rather than “SMA epilepsy” in optimal surgical candidates: a document of subdural mapping

Purpose: To clarify the relationship between epileptogenic zone and supplementary motor area (SMA) in patients who were regarded as the optimal surgical candidates for their intractable SMA seizures. Methods: We analyzed the epileptogenic zone at/or adjacent to the SMA in four patients with clinical SMA seizures. All four patients had noninvasive presurgical evaluations (long-term video/EEG monitoring, MRI, and neuroimaging with radioisotopes), which provided convergent results between ictal semiology and the epileptogenic area, and thus, they had chronically implanted subdural electrodes, and finally had focus resection with a follow-up period of more than 2 years. Results: Three patients had lesions shown by MRI outside the SMA, and one patient had a lesion within the SMA. Interictal epileptiform discharges were seen at/or outside the SMA. Ictal EEG pattern originated from the SMA in one patient, from the high lateral frontal area in two patients, and from the precuneus in one patient. In the latter three patients, the ictal EEG pattern immediately spread to the SMA. Those ictal onset zones were consistently localized within/or just adjacent to the lesions revealed by MRI. Only one patient had SMA resection, and three had the resection of epileptogenic zone by preserving the SMA. No neurological deficits developed and good seizure control was achieved. Conclusion: Among surgical candidates for intractable SMA seizures, frontal cortex other than SMA or even parietal cortex can be epileptogenic, and thus, the SMA itself may not necessarily have to be resected. This notion is clinically important when selecting surgical candidates as well as when planning presurgical invasive evaluation in patients with intractable SMA seizures.

Post operative supplementary motor area syndrome: clinical features and outcome

The syndrome of the supplementary motor area (SMA) is not well recognized and its features can easily be confused with pyramidal weakness. The authors describe the SMA syndrome in six patients who underwent surgery for tumours located in the SMA, three in the dominant and three in the non-dominant hemispheres. All of them underwent complete resection of the anatomically described SMA, with partial (n = 4) or total resection (n = 2) of the tumour. In the postoperative period, all these patients exhibited reduction of spontaneous movements and difficulty in performing voluntary motor acts to command in the contralateral limbs, although the tone in the limbs was maintained or increased. The function of these limbs in serial automatic motor activities (for example, dressing and walking) was, however, relatively unaffected. Speech deficits were seen in only one of three patients with the dominant SMA syndrome. Besides a severe impairment of volitional movements, the salient features of the deficits in this syndrome are hemineglect and dyspraxia or apraxia involving the contralateral limbs. All patients recovered their motor functions over varying periods of time ranging from one to a few weeks. Long-term follow-up (median 24 months) in five patients revealed complete return of function in the affected limbs. It is important to recognize the entity of the SMA syndrome and differentiate it from the deficits that result from operative damage to the motor cortex as the deficits associated with the former are likely to recover almost completely over a short period of time.

Functional results after resective procedures involving the supplementary motor area.

In this article, the authors report their experience with surgically induced supplementary motor area (SMA) deficiency syndrome in a prospective clinical trial of 28 patients who underwent surgery for tumorous (19 patients) or nontumorous (nine patients) lesions. The dominant side was affected in 17 patients and the nondominant side in 11 patients. The primary presenting symptoms included seizure activity (23 patients), hemiparesis (four patients), and aphasia (one patient). Functional topographic mapping, achieved by phase reversal of somatosensory evoked potentials, allowed precise localization of the central sulcus in 25 of the 28 patients. Motor evoked potential (MEP) monitoring, which was performed successfully in 13 of 15 cases during the resective procedure, showed no significant changes in the potentials in any patient. Immediately after surgery, 25 (89%) of the 28 patients displayed additional neurological deficits (aphasia and/or hemiparesis) that depended on the extent of the SMA resection. In 12 patients the SMA was resected completely: nine of these patients demonstrated a complete and three an incomplete deficit. In 16 patients the SMA resection was incomplete: 13 of these patients displayed an incomplete deficit, whereas three had no deficit. Neurological disorders resolved completely within 3 to 42 days (mean 11 days), except for a minimal disturbance of fine motor and/or speech function in complex tasks or at high speed. Electromagnetically elicited MEPs, examined postoperatively in five patients, were initially absent but recovered with improvement of motor function. In conclusion, although the SMA is known to control important functions such as initiation of motor activity or speech, our findings show that unilateral SMA removal can be accomplished without resulting in significant permanent deficits. Functional topographic mapping and monitoring facilitate the exact delineation of the adequate resection plane along the precentral sulcus, and postoperative magnetic resonance imaging allows precise correlation of clinical and anatomical data.