Supplementary Motor Area Syndrome Research Articles

SURG-19. THE SYNDROME OF THE SUPPLEMENTARY MOTOR AREA: CLINICAL COURSE AND PREDICTORS OF OUTCOME AFTER RESECTION OF PREMOTOR LESIONS

Abstract OBJECTIVE Supplementary motor area (SMA) syndrome frequently occurs after resection of premotor lesions. Interhemispheric connectivity including the contralateral SMA might be crucially involved in its development and recovery. We aimed to identify predictors of outcome by quantifying preoperative structural alterations in the non-affected contralateral hemisphere. METHODS We retrospectively searched our database for patients developing SMA syndrome after resection of premotor lesions between 2013 and 2023. Clinical characteristics and imaging data were collected. Structural network analysis was performed using the previously validated morphometric inverse divergence network. RESULTS 27 patients with a mean age of 39.2 ± 17.7 years developed SMA syndrome, including 13/27 patients (48.1%) with primary brain tumors and 14/27 patients (51.9%) with intractable lesional epilepsy. Postoperative SMA syndrome was commonly characterized by contralateral upper extremity hemiparesis (19/27 patients, 70.4%) and aphasia in case of dominant hemisphere involvement (13/13 patients, 100%). Tumor patients were less likely to fully recover from SMA syndrome after 7 days compared to epilepsy patients (2/13 [15.4%] versus 9/14 [64.3%] patients, p=0.018). Most patients (23/27, 85.2%) experienced full recovery of SMA syndrome after a median follow-up of 5 months (IR 3-16 months), with no difference between patients with tumors or epilepsy (p=0.999). Preoperative contralateral intra-hemispheric connectivity was similar between patients receiving tumor or focal resection (0.183 vs 0.177, p=0.295). However, imaging analyses demonstrated baseline affection of SMA connectivity in patients with brain tumors as characterized by reduced cortical thickness of the contralateral frontal lobe and the cingulate gyrus compared to epilepsy patients. CONCLUSION While full recovery from SMA syndrome is common, SMA syndrome is frequently less severe and more transient in patients with epilepsy. This might be due to affection of the contralateral SMA network in tumor patients due to the infiltrative nature of the disease. Imaging analyses might assist in identifying network affections at baseline.

Asymmetry of the Frontal Aslant Tract and Development of Supplementary Motor Area Syndrome

Background/Objectives: The purpose of this study was to investigate preoperative interhemispheric differences of the FAT in relation to the onset of postoperative SMA syndrome. Methods: This was a single-center retrospective analysis of patients who underwent surgical resection of diffuse gliomas involving the SMA between 2018 and 2022. Inclusion criteria were availability of preoperative and postoperative Magnetic Resonance Imaging, no previous surgery, and no neurological deficits at presentation. Diffusion-weighted data were processed by spherical deconvolution (SD) and diffusion tensor imaging tractography algorithms, and TrackVis was used to dissect the FAT of both hemispheres. The FAT data were analyzed for correlation with postoperative SMA syndrome onset. Results: N = 25 cases were included in the study, among which n = 23 had preoperative bilaterally identifiable FAT by SD. N = 12 developed an SMA syndrome, 6 demonstrated a motor-only syndrome, 4 had a verbal-only syndrome, and 2 had mixed verbal and motor features. The SMA syndrome incidence was significantly more frequent in lower-grade gliomas (p = 0.005). On the tumor side, the FAT identified by SD was smaller than the contralateral (mean volume 6.53 cm3 and 13.33 cm3, respectively, p < 0.001). In the 6 cases that developed a verbal SMA syndrome, a normalized FAT volume asymmetry (FAT-VA) demonstrated an asymmetry shifted towards the non-dominant side (mean FAT-VA = −0.68), while the cases with no postoperative verbal impairment had opposite asymmetry towards the dominant side (mean FAT-VA = 0.42, p = 0.010). Conclusions: Preoperative interhemispheric FAT volume asymmetry estimated according to functional dominance can predict postoperative onset of verbal SMA syndrome, with proportionally smaller FAT on the affected dominant hemisphere.

Postoperative Nodal Efficiency of the Lesional-Hemispheric Hand Motor Area Increasing Potentially Facilitated Motor Recovery for SMA Syndrome.

Supplementary motor area (SMA) syndrome commonly occurs after glioma resection and requires weeks to months of recovery. Thirty-four glioma patients with SMA syndrome were reviewed and assigned to recovered and non-recovered groups based on whether their motor function recovered on postoperative day 7. To validate the association between variations in nodal properties and recovery time, neuro-navigated repetitive transcranial magnetic stimulation (nrTMS) was applied to stimulate potential nodes. Nine other patients (five nrTMS therapy and four sham-nrTMS treatments) with SMA syndrome with unrecovered motor functions on postoperation day 7 were prospectively enrolled. The potential nodes of the sensorimotor network related to recovery time were investigated using preoperative and postoperative resting-state functional magnetic resonance imaging, graph theoretical analysis, and dynamic functional connectome analysis. Nodal efficiency of the lesional-hemispheric upper limb region of BA 4 (A4ul_L) increased in the recovered group (preoperative, 0.472 ± 0.027; postoperative, 0.535 ± 0.020; p = 0.0006). The patients in the nrTMS therapy group quickly recovered (12.0 ± 1.6 days) compared to the sham-nrTMS group (29.5 ± 3.8 days, p = 0.0024). Variations in A4ul_L nodal efficiency was negatively correlated with recovery time (r = -0.841; p = 0.0046). A4ul_L demonstrates enhanced postoperative nodal efficiency and shows therapeutic potential in SMA syndrome recovery, suggesting its viability as a therapeutic target.

“Apathetic look” is a valuable indicator of intraoperative supplementary motor area syndrome during awake craniotomy

“Apathetic look” is a valuable indicator of intraoperative supplementary motor area syndrome during awake craniotomy

Delayed Recovery of Bilateral Supplementary Motor Area Syndrome After the Resection of a Central Neurocytoma

Delayed Recovery of Bilateral Supplementary Motor Area Syndrome After the Resection of a Central Neurocytoma

Presentation, surgical outcome, and supplementary motor area syndrome risk of posterior superior frontal gyrus tumors.

Following resection of posterior superior frontal gyrus (PSFG) tumors, patients can experience supplementary motor area (SMA) syndrome consisting of contralateral hemiapraxia and/or speech apraxia. Given the heterogeneity of PSFG tumors, the authors sought to determine the risk of postoperative deficits and assess predictors of outcomes for all intraparenchymal PSFG tumors undergoing surgery (biopsy or resection), regardless of histology. This was a retrospective single-center cohort study of adult PSFG-region tumors undergoing biopsy or resection by a single surgeon. A total of 106 consecutive patients undergoing 123 procedures (21 biopsies, 102 resections) fulfilled inclusion and exclusion criteria. Anaplastic astrocytomas were the most frequent among resected tumors (39% vs 29%), while glioblastomas were most common among biopsies (38% vs 27%) (p < 0.0001). The biopsy cohort was more likely to have tumor involvement outside the PSFG (90% vs 62%) (p = 0.011), most commonly in the motor cortex (67% vs 31%) (p = 0.005). Seizures were the most common presenting symptom in the resection cohort (p = 0.017), while motor deficits were more common in the biopsy cohort (58% vs 29%) (p < 0.001). Immediate postoperative neurological deficits occurred in 71 cases (58%), but only 3 of the deficits were permanent at 6 months of follow-up (2%). Postoperative SMA syndrome occurred in 48 cases (47%) and was significantly associated with involvement of the motor cortex (p = 0.018) or cingulate gyrus (p = 0.023), which were also significant in multivariate analysis as risk factors for SMA syndrome. However, postoperative SMA syndrome was not significantly associated with overall survival (p = 0.51). There were no perioperative deaths, but corpus callosum involvement (p < 0.001), contrast enhancement (p = 0.003), and glioblastoma pathology (p = 0.038) predicted worse overall survival in patients undergoing resection. Nearly half of all patients undergoing resection of PSFG-region tumors experience a postoperative SMA syndrome. Individuals with corpus callosum and/or motor cortex involvement may be at an increased risk of experiencing SMA syndrome. However, these deficits are usually transient, and the risk of permanent new deficits is very low (3%). Preoperative characteristics including corpus callosum involvement and tumor enhancement-in addition to pathology-might serve as predictors of overall survival within this patient population.

Bilateral Supplementary Motor Area Syndrome Following Resection Of Parasagittal Large Brain Metastasis – A Case Report and Review of Literature

Bilateral Supplementary Motor Area Syndrome Following Resection Of Parasagittal Large Brain Metastasis – A Case Report and Review of Literature

Letter to the Editor Regarding: The Utility of Transcranial Electrical Stimulation Motor Evoked Potential Monitoring in Predicting Postoperative Supplementary Motor Area Syndrome and Motor Function Recovery

Letter to the Editor Regarding: The Utility of Transcranial Electrical Stimulation Motor Evoked Potential Monitoring in Predicting Postoperative Supplementary Motor Area Syndrome and Motor Function Recovery

In Reply to the Letter to the Editor Regarding: “The Utility of Transcranial Electrical Stimulation Motor Evoked Potential Monitoring in Predicting Postoperative Supplementary Motor Area Syndrome and Motor Function Recovery”

In Reply to the Letter to the Editor Regarding: “The Utility of Transcranial Electrical Stimulation Motor Evoked Potential Monitoring in Predicting Postoperative Supplementary Motor Area Syndrome and Motor Function Recovery”

Anatomical analysis of white fiber tracts in SMA and its implications related to en-masse tumor resection technique

ObjectiveAnatomy and connections of the supplementary motor area (SMA) are studied essentially to analyze the SMA syndrome. Experience with surgical treatment of 19 tumors located in SMA is analyzed. Material and MethodsThe cortical anatomy and subcortical connectivity of the SMA was studied on ten previously frozen and formalin fixed human cadaveric brain specimens. The white fiber dissection was performed using Klingler’s method. Nineteen patients with low grade gliomas in the region of the SMA treated surgically were clinically analyzed. ResultsThe white fiber connections of the SMA include short arcuate connections with the pre-central, middle and inferior frontal gyri, the medial part of the SLF, the cingulum, the frontal aslant tract (FAT), the claustro-cortical fibers, the fronto-striatal tract and the crossed frontal aslant tract. All tumors were operated using en-masse surgical technique described by us and its subsequent modifications that focused on attempts towards preservation of related critical fiber tracts namely FAT, cingulum and corpus callosum presumed to be responsible for postoperative SMA syndrome. Eight patients developed an SMA syndrome in the immediate post-operative period. Eleven patients did not develop any post-operative neurological deficits. In all these 11 patients it was apparent that the cingulum, FAT and the corpus callosal fibers were preserved during surgery by modifying the tumor resection technique. ConclusionsSMA syndrome is a frequent occurrence following surgery in patients with tumors in the region of the SMA complex. Surgical strategy that preserves the cingulum and the FAT can prevent the occurrence of the SMA syndrome.

Bilateral Supplementary Motor Area Syndrome Presenting with Functional Quadriparesis and Apraxia (P7-2.004)

Bilateral Supplementary Motor Area Syndrome Presenting with Functional Quadriparesis and Apraxia (P7-2.004)

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.

Supplementary Motor Area Syndrome After Resection of a Dominant Hemisphere Parasagittal Meningioma: A Case Report

BACKGROUND AND IMPORTANCE: Supplementary motor area (SMA) syndrome is a common, transient postoperative complication of intra-axial tumor resections involving the SMA and posterior cingulate gyrus. It is also reported as a rare complication of resecting extra-axial lesions. Meningiomas represent the most common, nonmalignant primary central nervous system tumor in adults, which present most commonly in parasagittal locations. Resection of dominant hemisphere parasagittal meningiomas overlying or infiltrating into the SMA region carry a recognizable risk for developing SMA syndrome postoperatively. CLINICAL PRESENTATION: We present a 58-year-old woman with intermittent headaches and concern for new-onset seizures. MRI demonstrated an extra-axial mass involving the left frontal convexity and SMA region with homogenous postcontrast enhancement. There was radiographic involvement of the superior sagittal sinus and inner table of the skull. Fluid-attenuated recovery signal and perilesional vasogenic edema were also noted. The imaging findings favored a parasagittal meningioma, and surgical resection was performed. Arachnoid invasion and pial infiltration of the tumor over the SMA were evident during the operation. CONCLUSION: A detailed understanding of the functional neuroanatomy and clinical pathophysiology of eloquent cortical regions is important for preoperative planning and patient counseling. Surgical resection of lesions in such areas can result in rare complications uniquely implicated in specific patient subsets. Recognizing these patients in the preoperative setting is imperative for proper counseling of patients and families.

Connectomics as a prognostic tool of functional outcome in glioma surgery of the supplementary motor area: illustrative case.

The supplementary motor area (SMA) is essential in facilitating the commencement and coordination of complex self-initiated movements. Its complex functional connectivity poses a great risk for postoperative neurological deterioration. SMA syndrome can occur after tumor resection and comprises hemiakinesia and akinetic mutism (often, but unpredictably temporary). Although awake surgery is preferred for mapping and monitoring eloquent areas, connectomics is emerging as a novel technique to tailor neurosurgical approaches and predict functional prognosis, as illustrated in this case. The authors report on a patient presenting with recurrent oligodendroglioma after subtotal resection 7 years earlier. After extensive neuropsychological and neuroradiological assessment (including connectomics), awake surgery was indicated. No intraoperative deficits were recorded; however, the patient presented with postoperative right-sided akinesia and mutism. Postoperative neuroimaging demonstrated the connectome overlapping the preoperative one, and indeed, neurological symptoms resolved after 3 days. Comparison of the pre- and postoperative connectome can be used to objectively evaluate surgical outcomes and assess patient prognosis. To the best of the authors' knowledge, this is the first case demonstrating the feasibility of quantitative functional connectivity analysis as a prognostic tool for neurological improvement after surgery. A better understanding of brain networks is instrumental for improving diagnosis, prognosis, and treatment of neuro-oncological patients.

Role of interhemispheric connectivity in recovery from postoperative supplementary motor area syndrome in glioma patients.

Surgical resection of gliomas involving the supplementary motor area (SMA) frequently results in SMA syndrome, a symptom complex characterized by transient akinesia and mutism. Because the factors influencing patient functional outcomes after surgery remain elusive, the authors investigated network-based predictors in a multicentric cohort of glioma patients. The participants were 50 patients treated for glioma located in the SMA at one of the three centers participating in the study. Postoperative functional outcomes (motor deficits, mutism) and duration of symptoms were assessed during hospitalization. Long-term outcome was assessed 3 months after surgery. MRI-based lesion-symptom mapping was performed to estimate the severity of gray matter damage and white matter disconnection. The median duration of acute symptoms was 3 days (range 1-42 days). Long-term deficits involving fine motor movements and speech were found at follow-up in 27 patients (54%). Disconnection of the central callosal fibers was associated with prolonged acute symptoms (p < 0.05). Postoperative mutism was significantly related to disconnection severity of the left frontopontine tract, frontal aslant tract, cingulum, and corticostriatal tract (p < 0.05). Disconnection of midposterior callosal fibers and lesion loads within the left medial Brodmann area 4 were associated with long-term motor deficits (p < 0.05). This study provides evidence for the pathophysiology and predictive factors of postoperative SMA syndrome by demonstrating the relation of the disconnection of callosal fibers with prolonged symptom duration (central segment) and long-term motor deficits (midposterior segment). These data may be useful for presurgical risk assessment and adequate consultation for patients prior to undergoing resection of glioma located within the SMA region.

Changes in Distributed Motor Network Connectivity Correlates With Functional Outcome After Surgical Resection of Brain Tumors

BACKGROUND: In patients with brain tumors around the motor cortices, deterioration of motor performance may be observed even if the integrity of the cortical output is maintained. Especially, resection of medial premotor area (PM) can cause postoperative deterioration called supplementary motor area syndrome. OBJECTIVE: To clarify the neuronal mechanisms underlying postsurgical deterioration with a case-control study. METHODS: Twelve patients with brain tumors underwent preoperative and postoperative sessions consisting of motor performance evaluation and 3T-magnetic resonance imaging data acquisition. Based on additional postsurgical motor deficits, 6 patients were classified into “deficit group,” and 6 others were into “no deficit group.” Using resting-state functional magnetic resonance imaging (fMRI), the integrity of functional connectivity was evaluated by placing a seed in the ipsilesional primary motor area (M1). With motor task fMRI, hand and foot representations were identified in the M1 and lateral and medial PMs. Probabilistic tractography assessed anatomic connectivity in the cortico-cortical and corticofugal networks. RESULTS: Functional connectivity among M1 and lateral and medial PMs during resting-state fMRI was reduced postoperatively in the deficit group (P &lt; .05, corrected) and preserved in the no deficit group. The deficit was unlikely to be attributable to surgical resection of specific anatomic connectivity. The amplitude of motor-evoked potential was maintained in available cases. These intraoperative observations agree with imaging findings suggesting preserved anatomic connectivity of the estimated corticofugal pathway. CONCLUSION: The present findings suggest that supplementary motor area syndrome is caused by disorganization of functional connectivity among cortical motor networks rather than resection of anatomic connectivity of corticofugal pathway.

ДОПОЛНИТЕЛЬНАЯ МОТОРНАЯ ОБЛАСТЬ И КЛИНИЧЕСКАЯ КАРТИНА ПРИ ЕЁ ПОРАЖЕНИИ

Methods: The supplementary motor area (SMA) is a cortical region, that is located on the medial surface of the frontal lobe entirely within the interhemispheric fissure between the primary motor cortex (PMC) and prefrontal cortex (PFC). This area is a heterogeneous region in its structure, as well as in its connections with other parts of the brain; on the basis of these differences, the pre-SMA and SMA-proper regions are distinguished in it. Numerous neural connections with other parts of the central nervous system (CNS) suggest the involvement of the SMA in many cognitive functions, and not only in higher motor ones, as previously was thought. In particular, in the dominant hemisphere, the SMA performs the speech function through the frontal oblique fascicle (FOF), a bundle of association fibers that connects the SMA with Broca's area. In the event of various pathologies affecting the SMA and after neurosurgical manipulations in this area, a variety of neurological disorders can occur both motor and verbal. With the damage of this cortical region in the dominant hemisphere, SMA syndrome (akinetic mutism) can occur. This paper provides a review of the anatomical, cytoarchitectonic, and functional features of the SMA, as well as a detailed description of the clinical picture of the lesion of this cortical region. Keywords: Brain, supplementary motor area, SMA syndrome.

Intra-Operative Supplementary Motor Area Aphosia During Awake Craniotomy a Case Report

Introduction: Language function is complex, involving association between Broca’s motor speech area, Wernicke’s sensory speech area and various interconnected cortical and sub-cortical regions. For lesions in eloquent areas, awake craniotomy with intra-operative neurological monitoring of motor and language function, aids in maximal safe resection of lesion with minimal neurological deficit. Case presentation: We present a case of 40-year-old patient with left frontal lobe lesion involving motor and speech area who underwent awake craniotomy under scalp block and titrated sedation. Though resection was in safe zone as marked both by neuro-navigation and direct electrical stimulation, patient developed aphasia intra-operatively. The aphasia resolved post-operatively with speech therapy over two weeks. Resection in Supplementary motor area (SMA) in the dominant hemisphere may be the likely cause of aphasia in this patient, resulting in reversible SMA syndrome. Conclusion: SMA syndrome must be considered as differential diagnosis of deficit during awake craniotomy when resection is in SMA. Keywords: Aphasia, Supplementary motor area, Awake craniotomy, Eloquent areas

STMO-14 VALIDATION OF SURGICAL METHODS FOR GLIOMA AROUND THE MOTOR CORTEX

Abstract Surgery for glioma around the primary motor area (primary MA) including premotor area (PA) and supplementary motor area (SMA) is performed by general anesthesia with motor evoked potential, called asleep surgery (Asleep S) or awake surgery (Awake S). The literature has shown that there is no difference in tumor removal rate and preservation of neurological function between the two methods. We retrospectively studied 14 patients who underwent craniotomy for glioma of the frontal lobe at our hospital, and 19 surgeries with contrast-enhancing lesions or T2 high-signal areas in the motor area. Tumor primary location was PMA: 6, PMA/ primary MA: 5, primary MA: 2, SMA 6 surgeries. All surgeries identified central sulcus by SEP and monitored transcranial and transcortical MEP. 11 surgeries were Asleep S and 8 were Awake S. Of the 11 Asleep S surgeries, 10 were high grade glioma with contrast on preoperative imaging. Of the 8 Awake S surgeries, 7 were lower grade gliomas, and most of these surgeries were performed for multiple recurrences. In Awake S, difficulties of assessment of motor function arose when the PMA and SMA were removed early in the surgery. In the case of Asleep S, to clarify the criteria for MEP warning signs is necessary, while in Awake S, the knowledge that how much motor decline is tolerated in voluntary movements need. In the case of Asleep S, to clarify the criteria for MEP warning signs is necessary, while in Awake S, the knowledge that how much motor decline is tolerated in voluntary movements need. In addition, the order of resection to avoid SMA syndrome and to evaluate motor function is important. We summarize the literatures and discuss these points for surgical strategy in glioma around motor area.

Surgical treatment of tumors of the supplementary motor area

Background. The supplementary motor area is a part of the medial frontal cortex, that is located just anterior to the primary motor cortex entirely within the interhemispheric fissure. This area belongs traditionally to the secondary motor cortex and perhaps it is the least studied motor region of the brain. While functions and symptoms of a damage to the primary motor and the premotor cortex areas have been well known and described for a long time, study of the supplementary motor area has been limited to fundamental neuroimaging and electrophysiological researches, and a practical side of the issue and clinical significance of this region remained outside the interest of researchers.Aim. To present the anatomical and functional features of the supplementary motor area, the clinical symptoms of its lesion, to analyze all the data available today and aspects of surgical treatment of tumors in this region.Materials and methods. A search in scientific databases (PubMed, etc.) led to the selection and analysis of sixty-two literary sources. The review is mainly devoted to the aspects and risk factors of surgical treatment of pathologies localized in this region.Results. According to its anatomical and functional characteristics, the supplementary motor area is a heterogeneous region - it has two separate subregions in it. In addition to the motor function of the supplementary motor area, its role has also been reliably established in the implementation of working memory processes, language, perceptual, cognitive and other functions. Such a number of functions performed by the supplementary motor area is associated with numerous neural connections of this area. For example, the frontal aslant tract has been described recently, and it connects medial part of the superior frontal gyrus with the pars opercularis of the inferior frontal gyrus. This tract, apparently, is associated with the implementation of language function in the dominant hemisphere and function of working memory in the non-dominant hemisphere.When the supplementary motor area is affected, various neurological motor and speech symptoms can occur, in particular, the supplementary motor area syndrome, which is characterized by the development of akinetic mutism in patients and, in most cases, is completely reversible within a few days or months. Among all pathologies in this area, tumors are most common, especially gliomas, which can also manifest themselves with various clinical symptoms both in the preoperative and postoperative periods.Conclusion. Critically important preoperative planning, informing the patient about the spatio-temporal picture of the predicted postoperative clinical disorders and the timing of rehabilitation are critically important. It is recommended to use methods of intraoperative neuronavigation, as well as intraoperative neurophysiological monitoring. It is necessary to further study the supplementary motor area and the peculiarities of its surgery in order to standardize approaches to the treatment of pathologies.