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Stephen T. Magill, Seunggu J. Han, Jing Li and Mitchel S. Berger

OBJECTIVE

Brain tumors involving the primary motor cortex are often deemed unresectable due to the potential neurological consequences that result from injury to this region. Nevertheless, we have challenged this dogma for many years and used asleep, as well as awake, intraoperative stimulation mapping to maximize extent of resection. It remains unclear whether these tumors can be resected with acceptable morbidity, whether performing the surgery with the patient awake or asleep impacts extent of resection, and how stimulation mapping influences outcomes.

METHODS

A retrospective chart review was performed on the senior author’s cohort to identify patients treated between 1998 and 2016 who underwent resection of tumors that were located within the primary motor cortex. Clinical notes, operative reports, and radiographic images were reviewed to identify intraoperative stimulation mapping findings and functional outcomes following tumor resection. Extent of resection was quantified volumetrically. Characteristics of patients were analyzed to identify factors associated with postoperative motor deficits.

RESULTS

Forty-nine patients underwent 53 resections of tumors located primarily within the motor cortex. Stimulation mapping was performed in all cases. Positive cortical sites for motor response were identified in 91% of cases, and subcortical sites in 74%. Awake craniotomy was performed in 65% of cases, while 35% were done under general anesthesia. The mean extent of resection was 91%. There was no statistically significant difference in extent of resection in cases done awake compared with those done under general anesthesia. New or worsened postoperative motor deficits occurred in 32 patients (60%), and 20 patients (38%) had a permanent deficit. Of the permanent deficits, 14 were mild, 4 were moderate, and 2 were severe (3.8% of cases). Decreased intraoperative motor response and diffusion restriction on postoperative MRI were associated with permanent deficit. Awake motor mapping surgery was associated with increased diffusion signal on postoperative MRI.

CONCLUSIONS

Resection of tumors from the primary motor cortex is associated with an increased risk of motor deficit, but most of these deficits are transient or mild and have little functional impact. Excellent extent of resection can be achieved with intraoperative stimulation mapping, suggesting that these tumors are indeed amenable to resection and should not be labeled unresectable. Injury to small perforating or en passage blood vessels was the most common cause of infarction that led to moderate or severe deficits. Awake motor mapping was not superior to mapping done under general anesthesia with regard to long-term functional outcome.

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Derek G. Southwell, Harjus S. Birk, Seunggu J. Han, Jing Li, Jeffrey W. Sall and Mitchel S. Berger

OBJECTIVE

Maximal safe resection is a primary objective in the management of gliomas. Despite this objective, surgeons and referring physicians may, on the basis of radiological studies alone, assume a glioma to be unresectable. Because imaging studies, including functional MRI, may not localize brain functions (such as language) with high fidelity, this simplistic approach may exclude some patients from what could be a safe resection. Intraoperative direct electrical stimulation (DES) allows for the accurate localization of functional areas, thereby enabling maximal resection of tumors, including those that may appear inoperable based solely on radiological studies. In this paper the authors describe the extent of resection (EOR) and functional outcomes following resections of tumors deemed inoperable by referring physicians and neurosurgeons.

METHODS

The authors retrospectively examined the cases of 58 adult patients who underwent glioma resection within 6 months of undergoing a brain biopsy of the same lesion at an outside hospital. All patients exhibited unifocal supratentorial disease and preoperative Karnofsky Performance Scale scores ≥ 70. The EOR and 6-month functional outcomes for this population were characterized.

RESULTS

Intraoperative DES mapping was performed on 96.6% (56 of 58) of patients. Nearly half of the patients (46.6%, 27 of 58) underwent an awake surgical procedure with DES. Overall, the mean EOR was 87.6% ± 13.6% (range 39.0%–100%). Gross-total resection (resection of more than 99% of the preoperative tumor volume) was achieved in 29.3% (17 of 58) of patients. Subtotal resection (95%–99% resection) and partial resection (PR; < 95% resection) were achieved in 12.1% (7 of 58) and 58.6% (34 of 58) of patients, respectively. Of the cases that involved PR, the mean EOR was 79.4% ± 12.2%. Six months after surgery, no patient was found to have a new postoperative neurological deficit. The majority of patients (89.7%, 52 of 58) were free of neurological deficits both pre- and postoperatively. The remainder of patients exhibited either residual but stable deficits (5.2%, 3 of 58) or complete correction of preoperative deficits (5.2%, 3 of 58).

CONCLUSIONS

The use of DES enabled maximal safe resections of gliomas deemed inoperable by referring neurosurgeons. With rare exceptions, tumor resectability cannot be determined solely by radiological studies.

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Derek G. Southwell, Marco Riva, Kesshi Jordan, Eduardo Caverzasi, Jing Li, David W. Perry, Roland G. Henry and Mitchel S. Berger

OBJECTIVE

The dominant inferior parietal lobule (IPL) contains cortical and subcortical regions essential for language. Although resection of IPL tumors could result in language deficits, little is known about the likelihood of postoperative language morbidity or the risk factors predisposing to this outcome.

METHODS

The authors retrospectively examined a series of patients who underwent resections of gliomas from the dominant IPL. Postoperative language outcomes were characterized across the patient population. To identify factors associated with postoperative language morbidity, the authors then compared features between those patients who experienced postoperative deficits and those who experienced no postoperative language dysfunction.

RESULTS

Twenty-four patients were identified for analysis. Long-term language deficits occurred in 29.2% of patients (7 of 24): 3 of these patients had experienced preoperative language deficits, whereas new long-term language deficits occurred in 4 patients (16.7%; 4 of 24). Of those patients who exhibited preoperative language deficits, 62.5% (5 of 8) experienced long-term resolution of their language deficits with surgical treatment. All patients underwent intraoperative brain mapping by direct electrical stimulation. Awake, intraoperative cortical language mapping was performed on 17 patients (70.8%). Positive cortical language sites were identified in 23.5% of these patients (4 of 17). Awake, intraoperative subcortical language mapping was performed in 8 patients (33.3%). Positive subcortical language sites were identified in 62.5% of these patients (5 of 8). Patients with positive cortical language sites exhibited a higher rate of long-term language deficits (3 of 4, 75%), compared with those who did not (1 of 13, 7.7%; p = 0.02). Although patients with positive subcortical language sites exhibited a higher rate of long-term language deficits than those who exhibited only negative sites (40.0% vs 0.0%, respectively), this difference was not statistically significant (p = 0.46). Additionally, patients with long-term language deficits were older than those without deficits (p < 0.05).

CONCLUSIONS

In a small number of patients with preoperative language deficits, IPL glioma resection resulted in improved language function. However, in patients with intact preoperative language function, resection of IPL gliomas may result in new language deficits, especially if the tumors are diffuse, high-grade lesions. Thus, language-dominant IPL glioma resection is not risk-free, yet it is safe and its morbidity can be reduced by the use of cortical and subcortical stimulation mapping.

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Eduardo Caverzasi, Shawn L. Hervey-Jumper, Kesshi M. Jordan, Iryna V. Lobach, Jing Li, Valentina Panara, Caroline A. Racine, Vanitha Sankaranarayanan, Bagrat Amirbekian, Nico Papinutto, Mitchel S. Berger and Roland G. Henry

OBJECT

Diffusion MRI has uniquely enabled in vivo delineation of white matter tracts, which has been applied to the segmentation of eloquent pathways for intraoperative mapping. The last decade has also seen the development from earlier diffusion tensor models to higher-order models, which take advantage of high angular resolution diffusion-weighted imaging (HARDI) techniques. However, these advanced methods have not been widely implemented for routine preoperative and intraoperative mapping.

The authors report on the application of residual bootstrap q-ball fiber tracking for routine mapping of potentially functional language pathways, the development of a system for rating tract injury to evaluate the impact on clinically assessed language function, and initial results predicting long-term language deficits following glioma resection.

METHODS

The authors have developed methods for the segmentation of 8 putative language pathways including dorsal phonological pathways and ventral semantic streams using residual bootstrap q-ball fiber tracking. Furthermore, they have implemented clinically feasible preoperative acquisition and processing of HARDI data to delineate these pathways for neurosurgical application. They have also developed a rating scale based on the altered fiber tract density to estimate the degree of pathway injury, applying these ratings to a subset of 35 patients with pre- and postoperative fiber tracking. The relationships between specific pathways and clinical language deficits were assessed to determine which pathways are predictive of long-term language deficits following surgery.

RESULTS

This tracking methodology has been routinely implemented for preoperative mapping in patients with brain gliomas who have undergone awake brain tumor resection at the University of California, San Francisco (more than 300 patients to date). In this particular study the authors investigated the white matter structure status and language correlation in a subcohort of 35 subjects both pre- and postsurgery. The rating scales developed for fiber pathway damage were found to be highly reproducible and provided significant correlations with language performance. Preservation of the left arcuate fasciculus (AF) and the temporoparietal component of the superior longitudinal fasciculus (SLF-tp) was consistent in all patients without language deficits (p < 0.001) at the long-term follow-up. Furthermore, in patients with short-term language deficits, the AF and/or SLF-tp were affected, and damage to these 2 pathways was predictive of a long-term language deficit (p = 0.005).

CONCLUSIONS

The authors demonstrated the successful application of q-ball tracking in presurgical planning for language pathways in brain tumor patients and in assessing white matter tract integrity postoperatively to predict long-term language dysfunction. These initial results predicting long-term language deficits following tumor resection indicate that postoperative injury to dorsal language pathways may be prognostic for long-term clinical language deficits.

Study results suggest the importance of dorsal stream tract preservation to reduce language deficits in patients undergoing glioma resection, as well as the potential prognostic value of assessing postoperative injury to dorsal language pathways to predict long-term clinical language deficits.

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Shawn L. Hervey-Jumper, Jing Li, Joseph A. Osorio, Darryl Lau, Annette M. Molinaro, Arnau Benet and Mitchel S. Berger

OBJECT

Though challenging, maximal safe resection of insular gliomas enhances overall and progression-free survival and deters malignant transformation. Previously published reports have shown that surgery can be performed with low morbidity. The authors previously described a Berger-Sanai zone classification system for insular gliomas. Using a subsequent dataset, they undertook this study to validate this zone classification system for predictability of extent of resection (EOR) in patients with insular gliomas.

METHODS

The study population included adults who had undergone resection of WHO Grade II, III, or IV insular gliomas. In accordance with our prior published report, tumor location was classified according to the Berger-Sanai quadrant-style classification system into Zones I through IV. Interobserver variability was analyzed using a cohort of newly diagnosed insular gliomas and independent classification scores given by 3 neurosurgeons at various career stages. Glioma volumes were analyzed using FLAIR and T1-weighted contrast-enhanced MR images.

RESULTS

One hundred twenty-nine procedures involving 114 consecutive patients were identified. The study population from the authors’ previously published experience included 115 procedures involving 104 patients. Thus, the total experience included 244 procedures involving 218 patients with insular gliomas treated at the authors’ institution. The most common presenting symptoms were seizure (68.2%) and asymptomatic recurrence (17.8%). WHO Grade II glioma histology was the most common (54.3%), followed by Grades III (34.1%) and IV (11.6%). The median tumor volume was 48.5 cm3. The majority of insular gliomas were located in the anterior portion of the insula with 31.0% in Zone I, 10.9% in Zone IV, and 16.3% in Zones I+IV. The Berger-Sanai zone classification system was highly reliable, with a kappa coefficient of 0.857. The median EOR for all zones was 85%. Comparison of EOR between the current and prior series showed no change and Zone I gliomas continue to have the highest median EOR. Short- and long-term neurological complications remain low, and zone classification correlated with short-term complications, which were highest in Zone I and in Giant insular gliomas.

CONCLUSIONS

The previously proposed Berger-Sanai classification system is highly reliable and predictive of insular glioma EOR and morbidity.

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Shawn L. Hervey-Jumper, Jing Li, Darryl Lau, Annette M. Molinaro, David W. Perry, Lingzhong Meng and Mitchel S. Berger

OBJECT

Awake craniotomy is currently a useful surgical approach to help identify and preserve functional areas during cortical and subcortical tumor resections. Methodologies have evolved over time to maximize patient safety and minimize morbidity using this technique. The goal of this study is to analyze a single surgeon's experience and the evolving methodology of awake language and sensorimotor mapping for glioma surgery.

METHODS

The authors retrospectively studied patients undergoing awake brain tumor surgery between 1986 and 2014. Operations for the initial 248 patients (1986–1997) were completed at the University of Washington, and the subsequent surgeries in 611 patients (1997–2014) were completed at the University of California, San Francisco. Perioperative risk factors and complications were assessed using the latter 611 cases.

RESULTS

The median patient age was 42 years (range 13–84 years). Sixty percent of patients had Karnofsky Performance Status (KPS) scores of 90–100, and 40% had KPS scores less than 80. Fifty-five percent of patients underwent surgery for high-grade gliomas, 42% for low-grade gliomas, 1% for metastatic lesions, and 2% for other lesions (cortical dysplasia, encephalitis, necrosis, abscess, and hemangioma). The majority of patients were in American Society of Anesthesiologists (ASA) Class 1 or 2 (mild systemic disease); however, patients with severe systemic disease were not excluded from awake brain tumor surgery and represented 15% of study participants. Laryngeal mask airway was used in 8 patients (1%) and was most commonly used for large vascular tumors with more than 2 cm of mass effect. The most common sedation regimen was propofol plus remifentanil (54%); however, 42% of patients required an adjustment to the initial sedation regimen before skin incision due to patient intolerance. Mannitol was used in 54% of cases. Twelve percent of patients were active smokers at the time of surgery, which did not impact completion of the intraoperative mapping procedure. Stimulation-induced seizures occurred in 3% of patients and were rapidly terminated with ice-cold Ringer's solution. Preoperative seizure history and tumor location were associated with an increased incidence of stimulation-induced seizures. Mapping was aborted in 3 cases (0.5%) due to intraoperative seizures (2 cases) and patient emotional intolerance (1 case). The overall perioperative complication rate was 10%.

CONCLUSIONS

Based on the current best practice described here and developed from multiple regimens used over a 27-year period, it is concluded that awake brain tumor surgery can be safely performed with extremely low complication and failure rates regardless of ASA classification; body mass index; smoking status; psychiatric or emotional history; seizure frequency and duration; and tumor site, size, and pathology.

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John D. Rolston, Dario J. Englot, Arnau Benet, Jing Li, Soonmee Cha and Mitchel S. Berger

OBJECT

The dominant hemisphere frontal operculum may contain critical speech and language pathways, and due to these properties, patients with tumors of the opercular region may be at higher risk for postoperative speech dysfunction. However, the likelihood of incurring temporary or permanent language dysfunction is unknown.

METHODS

The authors retrospectively analyzed their cohort of patients with frontal gliomas to identify those tumors that predominantly involved the dominant frontal operculum. Each tumor was classified as involving the pars orbitalis, pars triangularis, pars opercularis, or a combination of some or all of these areas. The authors then identified and compared characteristics between those patients experiencing transient or permanent speech deficits, as opposed to those with no language dysfunction.

RESULTS

Forty-three patients were identified for inclusion in this analysis. Transient deficits occurred in 12 patients (27.9%), while 4 patients (9.8%) had persistent deficits involving language. Individuals with preoperative language deficits and patients with seizures characterized by speech dysfunction appear to be at the highest risk to develop a deficit (relative risks 3.09 and 1.75, respectively). No patient with a tumor involving the pars orbitalis experienced a persistent deficit.

CONCLUSIONS

Resection of gliomas is widely recognized as a critical element of improved outcome. Given the low rate of language morbidity reported in this group of patients, resection of gliomas within the dominant frontal operculum is well-tolerated with acceptable morbidity and, in this particular location, should not be a deterrent in the overall management of these tumors.