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

J Neurosurg 136:1278–1284, 2022

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.

METHODS 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.

RESULTS 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).

CONCLUSIONS 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.

 

Gravity-assisted endoscopic cingulate gyrus glioma resection

Acta Neurochirurgica (2021) 163:1323–1326

The cingulate gyrus is part of the limbic systemwith extensive connectivity to different anatomical and functional areas. The traditional transcortical approach for a cingulate gyrus glioma contains high risk of transient or even irreversible postoperative hemiplegia.

Method We present a case of gravity-assisted, fully endoscopic resection of a cingulate gyrus glioma with improvement of motor dysfunction while preserving the paracentral lobule, corticospinal tracts, and supplementary motor area.

Conclusion This case demonstrates the value of gravity-assisted endoscopic resection in the dominant cingulate gyrus tumor which is surrounded by eloquent parenchyma.

A method for safely resecting anterior butterfly gliomas

J Neurosurg 126:1795–1811, 2017

Gliomas invading the anterior corpus callosum are commonly deemed unresectable due to an unacceptable risk/benefit ratio, including the risk of abulia. In this study, the authors investigated the anatomy of the cingulum and its connectivity within the default mode network (DMN). A technique is described involving awake subcortical mapping with higher attention tasks to preserve the cingulum and reduce the incidence of postoperative abulia for patients with so-called butterfly gliomas.

METHODS The authors reviewed clinical data on all patients undergoing glioma surgery performed by the senior author during a 4-year period at the University of Oklahoma Health Sciences Center. Forty patients were identified who underwent surgery for butterfly gliomas. Each patient was designated as having undergone surgery either with or without the use of awake subcortical mapping and preservation of the cingulum. Data recorded on these patients included the incidence of abulia/akinetic mutism. In the context of the study findings, the authors conducted a detailed anatomical study of the cingulum and its role within the DMN using postmortem fiber tract dissections of 10 cerebral hemispheres and in vivo diffusion tractography of 10 healthy subjects.

RESULTS Forty patients with butterfly gliomas were treated, 25 (62%) with standard surgical methods and 15 (38%) with awake subcortical mapping and preservation of the cingulum. One patient (1/15, 7%) experienced postoperative abulia following surgery with the cingulum-sparing technique. Greater than 90% resection was achieved in 13/15 (87%) of these patients.

CONCLUSIONS This study presents evidence that anterior butterfly gliomas can be safely removed using a novel, attention-task based, awake brain surgery technique that focuses on preserving the anatomical connectivity of the cingulum and relevant aspects of the cingulate gyrus.

 

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

Supplementary motor area

J Neurosurg 119:7–14, 2013

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.

Methods. 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.

Results. 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).

Conclusions. Resection of the cingulate gyrus in addition to the SMA was significantly associated with the development of postoperative neurological impairment.

The Contralateral Transcingulate Approach

Neurosurgery 71[ONS Suppl 1]:ons4–ons14, 2012

The contralateral transcingulate approach is a variation of the contralateral transcallosal approach for lesions located in the cingulate gyrus and deep white matter of the medial frontal lobe.

OBJECTIVE: To more thoroughly describe the contralateral transcingulate approach by reporting our operative technique and results.

METHODS: This approach positions the head with the midline horizontally, lesion on the upside, allowing gravity retraction of the dependent frontal lobe. Bifrontal craniotomy and splitting of the interhemispheric fissure create a crossing trajectory from the contralateral fissure to the ipsilateral cingulate gyrus that maximizes lateral exposure.

RESULTS: Eleven patients with vascular lesions were treated with the contralateral transcingulate approach (9 patients with cavernous malformations and 2 patients with arteriovenous malformations). Eight lesions were located on the left side, 5 in the cingulate gyrus, and 6 in the deep frontal lobe. The falx was cut in 5 patients to extend the crossing trajectory. All lesions were removed completely, with neurological morbidity in 1 patient caused by venous infarction.

CONCLUSION: Although similar to the contralateral transcallosal approach, the contralateral transcingulate approach accesses lesions outside the ventricle and has a steeper crossing trajectory. This approach requires no disruption of brain tissue with lesions on the cingulate surface and only a small incision in cingulate gyrus with lesions in the deep frontal lobe. The ipsilateral pericallosal and callosomarginal arteries provide dependable landmarks for transcingulate dissection. The contralateral transcingulate approach offers an alternative medial approach to lesions near language and motor areas and avoids lateral transcortical approaches, awake speech mapping, and risk to eloquent cortex in the dominant hemisphere.

Multicenter study on subcallosal cingulate DBS for depression

J Neurosurg 116:315–322, 2012. DOI: 10.3171/2011.10.JNS102122

Deep brain stimulation (DBS) has been recently investigated as a treatment for major depression. One of the proposed targets for this application is the subcallosal cingulate gyrus (SCG). To date, promising results after SCG DBS have been reported by a single center. In the present study the authors investigated whether these findings may be replicated at different institutions. They conducted a 3-center prospective open-label trial of SCG DBS for 12 months in patients with treatment-resistant depression.

Methods. Twenty-one patients underwent implantation of bilateral SCG electrodes. The authors examined the reduction in Hamilton Rating Scale for Depression (HRSD-17) score from baseline (RESP50).

Results. Patients treated with SCG DBS had an RESP50 of 57% at 1 month, 48% at 6 months, and 29% at 12 months. The response rate after 12 months of DBS, however, increased to 62% when defined as a reduction in the baseline HRSD-17 of 40% or more. Reductions in depressive symptomatology were associated with amelioration in disease severity in patients who responded to surgery.

Conclusions. Overall, findings from this study corroborate the results of previous reports showing that outcome of SCG DBS may be replicated across centers.

Deep brain stimulation of the subcallosal cingulate gyrus for depression

J Neurosurg 111:1209–1215, 2009.(DOI: 10.3171/2008.10.JNS08763)

Object. Deep brain stimulation (DBS) of the subcallosal cingulate gyrus (SCG), including Brodmann area 25, is currently being investigated for the treatment of major depressive disorder (MDD). As a potential emerging therapy, optimal target selection within the SCG has still to be determined. The authors compared the location of the electrode contacts in responders and nonresponders to DBS of the SCG and correlated the results with clinical outcome to help in identifying the optimal target within the region. Based on the location of the active contacts used for long-term stimulation in responders, the authors suggest a standardized method of targeting the SCG in patients with MDD.

Methods. Postoperative MR imaging studies of 20 patients with MDD treated with DBS of the SCG were ana- lyzed. The authors assessed the location of the active contacts relative to the midcommissural point and in relation to anatomical landmarks within the medial aspect of the frontal lobe. For this, a grid with 2 main lines was designed, with 1 line in the anterior-posterior and 1 line in the dorsal-ventral axis. Each of these lines was divided into 100 units, and data were converted into percentages. The anterior-posterior line extended from the anterior commissure (AC) to the projection of the anterior aspect of the corpus callosum (CCa). The dorsal-ventral line extended from the inferior portion of the CC (CCi) to the most ventral aspect of the frontal lobe (abbreviated “Fr” for the formula).

Results. Because the surgical technique did not vary across patients, differences in stereotactic coordinates between responders and nonresponders did not exceed 1.5 mm in any axis (x, y, or z). In patients who responded to the procedure, contacts used for long-term stimulation were in close approximation within the SCG. In the anterior- posterior line, these contacts were located within a 73.2 ± 7.7 percentile distance from the AC (with the AC center being 0% and the line crossing the CCa being 100%). In the dorsal-ventral line, active contacts in responders were located within a 26.2 ± 13.8 percentile distance from the CCi (with the CCi edge being 0% and the Fr inferior limit being 100%). In the medial-lateral plane, most electrode tips were in the transition between the gray and white matter of SCG.

Conclusions. Active contacts in patients who responded to DBS were relatively clustered within the SCG. Be- cause of the anatomical variability in the size and shape of the SCG, the authors developed a method to standardize the targeting of this region.