Permanent deterioration of fine motor skills after the resection of tumors in the supplementary motor area.

Supplementary motor area syndrome (SMAS) represents a common neurosurgical sequela. The incidence and time frame of its occurrence have yet to be characterized after surgery for brain tumors. We examined patients suffering from a brain tumor preoperatively, postoperatively, and during follow-up examinations after three months, including fine motor skills testing and transcranial magnetic stimulation (TMS). 13 patients suffering from a tumor in the dorsal part of the superior frontal gyrus underwent preoperative, early postoperative, and 3-month follow-up testing of fine motor skills using the Jebsen-Taylor Hand Function Test (JHFT) and the Nine-Hole Peg Test (NHPT) consisting of 8 subtests for both upper extremities. They completed TMS for cortical motor function mapping. Test completion times (TCTs) were recorded and compared. No patient suffered from neurological deficits before surgery. On postoperative day one, we detected motor deficits in two patients, which remained clinically stable at a 3-month follow-up. Except for page-turning, every subtest indicated a significant worsening of function, reflected by longer TCTs (p < 0.05) in the postoperative examinations for the contralateral upper extremity (contralateral to the tumor manifestation). At 3-month follow-up examinations for the contralateral upper extremity, each subtest indicated significant worsening compared to the preoperative status despite improvement to the immediate postoperative level. We also detected significantly longer TCTs (p < 0.05) postoperatively in the ipsilateral upper extremity. This study suggests a long-term worsening of fine motor skills even three months after SMA tumor resection, indicating the necessity of targeted physical therapy for these patients.

The Utility of Transcranial Electrical Stimulation Motor Evoked Potential Monitoring in Predicting Postoperative Supplementary Motor Area Syndrome and Motor Function Recovery.

BACKGROUND: Postoperative hemiparesis following frontal lobe lesion resection is alarming, and predicting motor function recovery is challenging. Supplementary motor area (SMA) syndrome following resection of frontal lobe lesions is often indistinguishable from postoperative motor deficit due to surgical injury of motor tracts. We aimed to describe the use of intraoperative transcranial electrical stimulation (TES) with motor evoked potential monitoring data as a diagnostic tool to distinguish between SMA syndrome and permanent motor deficit (PMD). METHODS: A retrospective analysis of 235 patients undergoing craniotomy and resection with TES-MEP monitoring for a frontal lobe lesion was performed. Patients who developed immediate postoperative motor deficit were included. Motor deficit and TES-MEP findings were categorized by muscle group as left upper extremity, left lower extremity, right upper extremity, or right lower extremity. Statistical analysis was performed to determine the predictive value of stable TES-MEP for SMA syndrome versus PMD. RESULTS: This study included 20 patients comprising 29 cases of immediate postoperative motor deficit by muscle group. Of these, 27 cases resolved and were diagnosed as SMA syndrome, and 2 cases progressed to PMD. TES-MEP stability was significantly associated with diagnosis of SMA syndrome (P = 0.015). TES-MEP showed excellent diagnostic utility with a sensitivity and positive predictive value of 100% and 92.6%, respectively. Negative predictive value was 100%. CONCLUSIONS: Temporary SMA syndrome is difficult to distinguish from PMD immediately postoperatively. TES-MEP may be a useful intraoperative adjunct that may aid in distinguishing SMA syndrome from PMD secondary to surgical injury.

Impact of augmented reality fiber tractography on the extent of resection and functional outcome of primary motor area tumors.

OBJECTIVE: This study aimed to evaluate the impact of augmented reality intraoperative fiber tractography (AR-iFT) on extent of resection (EOR), motor functional outcome, and survival of patients with primary motor area (M1) intra-axial malignant tumors. METHODS: Data obtained from patients who underwent AR-iFT for M1 primary tumors were retrospectively analyzed and compared with those from a control group who underwent unaugmented reality intraoperative fiber tractography (unAR-iFT). A full asleep procedure with electrical stimulation mapping and fluorescein guidance was performed in both groups. The Neurological Assessment in Neuro-Oncology (NANO), Medical Research Council (MRC), and House-Brackmann grading systems were used for neurological, motor, and facial nerve assessment, respectively. Three-month postoperative NANO and MRC scores were used as outcome measures of the safety of the technique, whereas EOR and survival curves were related to its cytoreductive efficacy. In this study, p < 0.05 indicated statistical significance. RESULTS: This study included 34 and 31 patients in the AR-iFT and unAR-iFT groups, respectively. The intraoperative seizure rate, 3-month postoperative NANO score, and 1-week and 1-month MRC scores were significantly (p < 0.05) different and in favor of the AR-iFT group. However, no difference was observed in the rate of complications. Glioma had incidence rates of 58.9% and 51.7% in the study and control groups, respectively, with no statistical difference. Metastasis had a slightly higher incidence rate in the control group, without statistical significance, and the gross-total resection and near-total resection rates and progression-free survival (PFS) rate were higher in the study group. Overall survival was not affected by the technique. CONCLUSIONS: AR-iFT proved to be feasible, effective, and safe during surgery for M1 tumors and positively affected the EOR, intraoperative seizure rate, motor outcome, and PFS. Integration with electrical stimulation mapping is critical to achieve constant anatomo-functional intraoperative feedback. The accuracy of AR-iFT is intrinsically limited by diffusion tensor-based techniques, parallax error, and fiber tract crowding. Further studies are warranted to definitively validate the benefits of augmented reality navigation in this surgical scenario.

Intraoperative Augmented Reality Fiber Tractography for Primary Motor Area Glioma Resection.

The implementation of intraoperative augmented reality fiber tractography (iAR-FT) into the surgical workflow for high-grade supratentorial gliomas has been shown to be effective and safe in maximizing the extent of resection and progression-free survival through the surgeon's enhanced 3-dimensional awareness of the spatial localization of fiber tracts.1-3 Primary motor area tumors present special challenges due to the high eloquence of the precentral gyrus and risk of postoperative onset or worsening of motor deficits, as well as limited postoperative plasticity.4 Although essential, electrical stimulation mapping (ESM) techniques have a number of limitations with respect to primary motor pathways, including a higher risk of intraoperative stimulation-evoked seizures, a risk of false negatives in the presence of preoperative deficits, a nonnegligible risk of permanent deterioration even in the presence of negative stimulation maps, and, most importantly, limited spatial resolution.4-8 The rationale for integrating ESM and iAR-FT is to compensate for the limitations of the former in terms of morphologic and spatial representation of fiber tracts. The benefits of coupling iAR-FT with ESM techniques allow for continuous integrated anatomical-functional feedback during surgery. In Video 1 we describe the key technical aspects and benefits of iAR-FT-assisted surgery for maximal safe gross total resection of a primary motor area grade IV astrocytoma.

Positioning of epidural electrode for motor cortex stimulation in general anesthesia based on intraoperative electrophysiological monitoring to treat refractory trigeminal neuropathic pain.

BACKGROUND: Motor cortex stimulation (MCS) represents a treatment option for refractory trigeminal neuralgia (TGN). Usually, patients need to be awake during surgery to confirm a correct position of the epidural electrode above the motor cortex, reducing patient's comfort. METHOD: Epidural cortical mapping (ECM) and motor evoked potentials (MEPs) were intraoperatively performed for correct localization of motor cortex under general anesthesia that provided comparable results to test stimulation after letting the patient to be awake during the operation. CONCLUSION: Intraoperative ECM and MEPs facilitate a confirmation of correct MCS-electrode position above the motor cortex allowing the MCS-procedure to be performed under general anesthesia.

[Surgical treatment of tumors of the supplementary motor area]. / Khirurgicheskoe lechenie opukholei dopolnitel'noi motornoi oblasti.

After surgical treatment of tumors of the supplementary motor area (SMA) post-operative speech and/or motor neurological deficit may occur. OBJECTIVE: To determinate frequency and reversibility of such deficit and identify risk factors for its development. MATERIAL AND METHODS: We retrospectively analyzed postoperative outcomes in 34 patients with SMA tumors. Pre- and postoperative neurological status, localization of tumors, extent of resection relative to adjacent regions and relationship of tumor with white matter tracts were assessed. We also analyzed the influence of these factors on the risk of postoperative neurological impairment. RESULTS: Postoperative neurological impairment occurred in 47% of cases. Complete or significant regression was observed in all patients within 5.7 month after surgery. Major risk factors were lesion of dominant hemisphere (p=0.029), tumor spreading to primary motor cortex (p=0.018) and resection of SMA together with cingulate gyrus (p=0.000). Location of frontal aslant tract in dominant hemisphere just near the tumor contributed to disorders regarding speech initiation and fluency (p=0.016). Resection of SMA with cingulate gyrus in dominant hemisphere affected development of more serious speech disorders (p=0.003). CONCLUSION: Surgery for SMA tumors is safe and followed by favorable functional outcomes.

Two cases of SMA syndrome after neurosurgical injury to the frontal aslant tract.

Supplementary motor area (SMA) syndrome is characterised by transient disturbance in volitional movement and speech production which classically occurs after injury to the medial premotor area. We present two cases of SMA syndrome following isolated surgical injury to the frontal aslant tract (FAT) with the SMA intact. The first case occurred after resection of a left frontal operculum tumour. The second case occurred after a transcortical approach to a ventricular neurocytoma. The clinical picture and fMRI activation patterns during recovery were typical for SMA syndrome and support the theory that the FAT is a critical bundle in the SMA complex function.

MRI-guided focused-ultrasound thalamotomy in essential tremor: Immediate and delayed changes in cortico-muscular coherence and cortico-cortical out-strength.

OBJECTIVE: Drug-resistant essential tremor (ET) can be treated by Magnetic-Resonance-guided Focused-Ultrasound (MRgFUS) targeted to thalamic ventralis-intermediate nucleus (ViM). We are presenting the results obtained in ET patients by evaluating the cortico-muscular coherence (CMC) and the out-strength among cortical areas. METHODS: We recorded MEG-EMG signals in 16 patients with predominant tremor on the right upper limb. The examination was performed the day before MRgFUS (T0) treatment, 24 hours (T1), and 3-months (T2) after lesioning the left ViM. Normalized CMC (nCMC) and cortico-cortical out-strength among cortical areas were assessed during isometric extension of the right hand. RESULTS: According to the Essential Tremor Rating Assessment Scale, 13 of 16 patients were considered responders. At T1, in the beta-band, nCMC increased in the left hemisphere, namely in the areas directly involved in motor functions. At T2, the nCMC in non-motor areas decreased and the out-strength from other examined cortical areas toward the left motor-area decreased. CONCLUSIONS: In patients positively responding to MRgFUS, the CMC increased in the motor-area of the treated hemisphere immediately after the treatment, while the reorganization of CMC and cortico-cortical out-strength toward the cortical motor area occurred with a delay. SIGNIFICANCE: The effective treatment with MRgFUS corresponds with a readjustment of the CMC and of the communication between cortical areas.

Features of the Sensorimotor Cortex Altered after Tooth Loss and Subsequent Implant Placement in the Maxilla of Rats.

OBJECTIVE: To investigate the synergistic changes of the astrocytes and neurons in the sensorimotor cortex during the process of implant osseointegration after insertion. METHODS: A total of 75 rats were allocated into three groups (n = 25): non-operated, extraction and implant. The rats in the latter two groups underwent extraction surgery of three maxillary right molars. One month later, the implant group received one titanium implant in the healed extraction socket. The rats were sacrificed on days 1, 3, 7, 14 and 28 after implantation. The brain sections, including sensory centre S1 and motor centre M1, were selected for further immunofluorescence for measurement of the synergistic morphological and quantitative changes of astrocytes and neurons. RESULTS: In layer IV of S1, the number of astrocytes in the implant group showed a descending trend with time; on days 1, 3, 7 and 14, the number of astrocytes in both the extraction group and the implant group was significantly higher than that in the non-operated group, and there was no difference between the extraction group and the implant group; however, on day 28, the number of astrocytes in the implant group was significantly lower than that in the extraction group. In layer V of M1, on days 7, 14 and 28, the number of astrocytes in the implant group was significantly lower than that in the extraction group; on days 14 and 28, the number of astrocytes in the extraction group was significantly higher than that in the non-operated group. In layer IV of S1 or layer V of M1, the number of neurons showed no significant changes between the three groups. CONCLUSION: The astrocytes in the face sensorimotor cortex were activated as a reaction to oral environment changes. This kind of neuroplasticity can be reversed by oral rehabilitation with dental implants. The motor cortex may be intimately related to osseointegration and osseoperception.

[Comparison of resting state and task-based functional MRI in preoperative mapping in patients with brain gliomas]. / Sravnenie funktsional'noi magnitno-rezonansnoi tomografii v sostoyanii pokoya i stimul-zavisimoi funktsional'noi magnitno-rezonansnoi tomografii v predoperatsionnom kartirovanii u patsientov s gliomami golovnogo mozga.

OBJECTIVE: To analyze and compare the results of cerebral cortex mapping with task-based (tb-fMRI) and resting-state functional MRI in patients with glioma of eloquent cortical areas. MATERIAL AND METHODS: There were 55 patients (24 men and 31 women aged 24 - 74 years, median 39) with glial tumors. In 26 patients, the tumor was located in motor areas. Twenty-nine patients had lesions of Broca and Wernicke's areas. All patients underwent preoperative tb-fMRI and rs-fMRI. Then, resection of tumor was carried out in all cases. RESULTS: Comparison of fMRI and rs-fMRI activation maps was assessed by calculating the Dice coefficient for inclusive speech and motor cortex masks and exclusive masks without brainstem, cerebellum, subcortical nuclei. Inclusive Dice coefficient for motor cortex ranged from 0.11 to 0.50, for speech cortex - from 0.006 to 0.240 (p<0.05). In case of exclusive masks, this value ranged from 0.15 to 0.55 for motor cortex and from 0.004 to 0.205 for speech cortex (p<0.05). CONCLUSION: When comparing the results of cortical mapping in patients with glial tumors, the use of hemispheric exclusive and inclusive masks did not significantly increase activation maps matching. Probably, low degree of correspondence was associated with different genesis of activations, as well as with high variability of speech cortex.

Supplementary Motor Area Syndrome after Removal of an Unusual Extensive Parasagittal Meningioma: Analysis of Twelve Reported Cases.

Background and Objectives: Supplementary motor area (SMA) syndrome is a common post-operation complication in intra-axial brain tumors, such as glioma. Direct damage to parenchyma or scarification of the major vessels during an operation are the main causes. However, it is rarely reported as a postoperative complication in extra-axial tumors. Materials and Methods: We reviewed 11 reported cases of supplementary motor area syndrome after removal of extra-axial meningiomas in the English literature from the PubMed database. We also added our case, which presented as an unusual huge meningioma, to analyze the clinical parameters and outcomes of these 12 reported cases. Results: Recovery time of supplementary motor area syndrome in extra-axial tumors could be within 1-7 weeks, shorter than intra-axial tumors (2-9 weeks). Epilepsy and progressive limb weakness are the most common presentations in 50% of cases. Different degrees of postoperative muscle power deterioration were noted in the first 48 h (from 0-4). Lower limbs (66.6%, 8/12) were slightly predominant compared to upper limbs (58.3%, 7/12). Mutism aphasia was also observed in 41.6% (5/12, including our case), and occurred in tumors which were involved in the dominant side; this recovered faster than limb weakness. Discussion and Conclusions: Our work indicated that SMA syndrome could occur in extra-axial brain tumors presenting as mutism aphasia and limb weakness without any direct brain parenchyma damage. In our analysis, we found that recovery time of postoperative motor function deficit could be within 1-7 weeks. Our study also provides a further insight of SMA syndrome in extra-axial brain tumors.

Supplementary Motor Area Syndrome After Brain Tumor Surgery: A Systematic Review.

BACKGROUND: Supplementary motor area syndrome (SMAS) may occur after frontal tumor surgery, with variable presentation and outcomes. We reviewed the literature on postoperative SMAS after brain tumor resection. METHODS: PubMed, Web of Science, Scopus, and Cochrane were searched following the PRISMA guidelines to include studies reporting SMAS after brain tumor resection. RESULTS: We included 31 studies encompassing 236 patients. Most tumors were gliomas (94.5%), frequently of low grade (61.4%). Most lesions were located on the left hemisphere (64.4%), involving the supplementary motor area (61.4%) and the cingulate gyrus (20.8%). Tractography and functional magnetic resonance imaging evaluation were completed in 45 (19.1%) and 26 (11%) patients. Gross total resection was achieved in 46.3% patients and complete SMA resection in 69.4%. A total of 215 procedures (91.1%) used intraoperative neuromonitoring mostly consisting of direct cortical/subcortical stimulation (56.4%), motor (33.9%), and somatosensory (25.4%) evoked potentials. Postoperative SMAS symptoms occurred within 24 hours after surgery, characterized by motor deficits (97%), including paresis (68.6%) and hemiplegia (16.1%), and speech disorders (53%), including hesitancy (24.2%) and mutism (22%). Average SMAS duration was 45 days (range, 1-365 days), with total resolution occurring in 188 patients (79.7%) and partial improvement in 46 (19.5%). Forty-eight patients (20.3%) had persisting symptoms, mostly speech hesitancy (60.4%) and fine motor disorders (45.8%). CONCLUSIONS: Postoperative SMAS may occur within the first 24 hours after mesial frontal tumor surgery. Preoperative mapping and intraoperative neuromonitoring may assist resection and predict outcomes. Neuroplasticity and interhemispheric connectivity play a major role in resolution.

Single-stage resection of bottom-of-a-sulcus dysplasia involving eloquent cortex using navigated transcranial magnetic stimulation and intraoperative modalities.

BACKGROUND: Focal cortical dysplasia (FCD) is a common etiology of refractory epilepsy, particularly in children. Surgical management is potentially curative, but poses the challenge of distinguishing the border between ictogenic regions of dysplasia and functionally critical brain tissue. Bottom-of-a-sulcus dysplasia (BOSD) amplifies this challenge, due to difficulties in physiologic mapping of the deep tissue. METHODS: We report a one-stage resection of a dysplasia-associated seizure focus abutting and involving the hand and face primary motor cortex. In doing so, we describe our surgical planning integrating neuronavigated transcranial magnetic stimulation (nTMS) for functional motor mapping, combined with intraoperative ultrasonography, intracranial electroencephalography, and magnetic resonance imaging (MRI). A 5-year-old girl with intractable focal epilepsy was referred to our comprehensive epilepsy program. Despite attentive pharmacotherapy, she experienced status epilepticus and up to 70 seizures per day, accompanied by multiple side effects from her antiseizure medication. A right frontal BOSD in close proximity to the hand motor area of the precentral gyrus was identified on MRI. Postoperatively, she is seizure-free for over 1 year with no hand deficit. CONCLUSION: Although technically complex, single-stage resection taking advantage of comprehensive surgical planning with optimized fusion of functional mapping and intraoperative modalities merits consideration given the invasiveness of a two-stage approach for limited added value. Integrated pre-surgical nTMS allowed for mapping of eloquent cortex without invasive electrocortical stimulation.

Awake Surgery for Local Recurrence of Brain Metastasis in the Precentral Gyrus After Fractionated Stereotactic Radiotherapy: A Technical Case Report.

BACKGROUND: To avoid permanent neurologic deficits and preserve brain function, intraoperative electrical stimulation mapping (IESM) is essential for surgical resection. CASE REPORT: A 59-year-old right-handed woman with ovarian cancer who had undergone stereotactic radiotherapy for brain metastasis two years before, was introduced due to progressive left upper paresis. Magnetic resonance imaging showed a recurrence of the lesion. We performed awake surgery using IESM. Thus, the sensorimotor site was elicited on the precentral and postcentral gyrus. However, IESM elicited no disturbance of motor function on the surface of the posterior part of the precentral gyrus. We made a safe corticotomy on it, and performed the resection of recurrent BM. Preserving the motor and sensory function, we achieved the resection of BM. After surgery, she experienced a significant improvement in motor function. CONCLUSION: IESM is a useful tool to make a safe approach via the precentral gyrus avoiding permanent sensorimotor deficits.