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Derek G. Southwell, Shawn L. Hervey-Jumper, David W. Perry, and Mitchel S. Berger

OBJECT

To avoid iatrogenic injury during the removal of intrinsic cerebral neoplasms such as gliomas, direct electrical stimulation (DES) is used to identify cortical and subcortical white matter pathways critical for language, motor, and sensory function. When a patient undergoes more than 1 brain tumor resection as in the case of tumor recurrence, the use of DES provides an unusual opportunity to examine brain plasticity in the setting of neurological disease.

METHODS

The authors examined 561 consecutive cases in which patients underwent DES mapping during surgery forglioma resection. “Positive” and “negative” sites—discrete cortical regions where electrical stimulation did (positive) or did not (negative) produce transient sensory, motor, or language disturbance—were identified prior to tumor resection and documented by intraoperative photography for categorization into functional maps. In this group of 561 patients, 18 were identified who underwent repeat surgery in which 1 or more stimulation sites overlapped with those tested during the initial surgery. The authors compared intraoperative sensory, motor, or language mapping results between initial and repeat surgeries, and evaluated the clinical outcomes for these patients.

RESULTS

A total of 117 sites were tested for sensory (7 sites, 6.0%), motor (9 sites, 7.7%), or language (101 sites, 86.3%) function during both initial and repeat surgeries. The mean interval between surgical procedures was 4.1 years. During initial surgeries, 95 (81.2%) of 117 sites were found to be negative and 22 (18.8%) of 117 sites were found to be positive. During repeat surgeries, 103 (88.0%) of 117 sites were negative and 14 (12.0%) of 117 were positive. Of the 95 sites that were negative at the initial surgery, 94 (98.9%) were also negative at the repeat surgery, while 1 (1.1%) site was found to be positive. Of the 22 sites that were initially positive, 13 (59.1%) remained positive at repeat surgery, while 9 (40.9%) had become negative for function. Overall, 6 (33.3%) of 18 patients exhibited loss of function at 1 or more motor or language sites between surgeries. Loss of function at these sites was not associated with neurological impairment at the time of repeat surgery, suggesting that neurological function was preserved through neural circuit reorganization or activation of latent functional pathways.

CONCLUSIONS

The adult central nervous system reorganizes motor and language areas in patients with glioma. Ultimately, adult neural plasticity may help to preserve motor and language function in the presence of evolving structural lesions. The insight gained from this subset of patients has implications for our understanding of brain plasticity in clinical settings.

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Edward F. Chang, Doris D. Wang, David W. Perry, Nicholas M. Barbaro, and Mitchel S. Berger

Object

Language dominance in the right hemisphere is rare. Therefore, the organization of essential language sites in the dominant right hemisphere is unclear, especially compared with cases involving the more prevalent left dominant hemisphere.

Methods

The authors reviewed the medical records of 15 patients who underwent awake craniotomy for tumor or epilepsy surgery and speech mapping of right hemisphere perisylvian language areas at the University of California, San Francisco. All patients were determined to have either complete right-sided or bilateral language dominance by preoperative Wada testing.

Results

All patients but one were left-handed. Of more than 331 total stimulation sites, 27 total sites were identified as essential for language function (14 sites for speech arrest/anarthria; 12 for anomia; and 1 for alexia). While significant interindividual variability was observed, the general pattern of language organization was similar to classic descriptions of frontal language production and posterior temporal language integration for the left hemisphere. Speech arrest sites were clustered in the ventral precentral gyrus and pars opercularis. Anomia sites were more widely distributed, but were focused in the posterior superior and middle temporal gyri as well as the inferior parietal gyrus. One alexia site was found over the superior temporal gyrus. Face sensory and motor cortical sites were also identified along the ventral sensorimotor strip. The prevalence and specificity of essential language sites were greater in unilateral right hemisphere–dominant patients, compared with those with bilateral dominance by Wada testing.

Conclusions

The authors' results suggest that the organization of language in right hemisphere dominance mirrors that of left hemisphere dominance. Awake speech mapping is a safe and reliable surgical adjunct in these rare clinical cases and should be done in the setting of right hemisphere dominance to avoid preventable postoperative aphasia.

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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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Michael D. Szymanski, David W. Perry, Nicole M. Gage, Howard A. Rowley, John Walker, Mitchel S. Berger, and Timothy P. L. Roberts

Object. The goal of this study was to determine whether the late neuromagnetic field elicited by simple speech sounds, which is detected by magnetoencephalography, may be used to estimate hemispheric dominance for language and to guide or constrain the intraoperative search for essential language sites. If sufficiently robust, a noninvasive method for assessing hemispheric dominance for language could reduce the necessity for amobarbital testing and the extent of intraoperative cortical stimulation—based mapping, both of which carry the risk of morbidity.

Methods. Fifteen patients undergoing surgery for tumors during which intraoperative language mapping would be performed and two additional patients in whom intracarotid amobarbital testing confirmed right-hemisphere language dominance participated. Following a primary auditory response sources of late neuromagnetic fields elicited by vowel stimuli were modeled and coregistered using magnetic resonance images to form magnetic source (MS) images. A laterality index (LI) was calculated by summing the number of equivalent current dipolar sources in the late fields detected from each hemisphere. In 14 right-handed patients, 10 displayed left asymmetric LIs (0.37 ± 0.16, mean ± standard error of the mean in 14 patients). For both right-hemisphere dominant patients in whom an LI was obtainable, the LI was rightward. Stimulation-mapped essential language sites were found in 7 of 15 patients. For six of these seven patients, the MS image—derived LI was leftward.

Conclusions. Asymmetry in single equivalent dipole modeling of the late neuromagnetic field evoked by simple speech sounds correlates with hemispheric language dominance, although not to the degree necessary for individual clinical predictions. With further development, MS imaging of simple language tasks may be used preoperatively to predict language dominance and even to identify or constrain the intraoperative search for likely sites of essential language cortex.

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Stephen M. Wilson, Daniel Lam, Miranda C. Babiak, David W. Perry, Tina Shih, Christopher P. Hess, Mitchel S. Berger, and Edward F. Chang

OBJECT

Transient aphasias are often observed in the first few days after a patient has undergone resection in the language-dominant hemisphere. The aims of this prospective study were to characterize the incidence and nature of these aphasias and to determine whether there are relationships between location of the surgical site and deficits in specific language domains.

METHODS

One hundred ten patients undergoing resection to the language-dominant hemisphere participated in the study. Language was evaluated prior to surgery and 2–3 days and 1 month postsurgery using the Western Aphasia Battery and the Boston Naming Test. Voxel-based lesion-symptom mapping was used to identify relationships between the surgical site location assessed on MRI and deficits in fluency, information content, comprehension, repetition, and naming.

RESULTS

Seventy-one percent of patients were classified as aphasic based on the Western Aphasia Battery 2–3 days postsurgery, with deficits observed in each of the language domains examined. Fluency deficits were associated with resection of the precentral gyrus and adjacent inferior frontal cortex. Reduced information content of spoken output was associated with resection of the ventral precentral gyrus and posterior inferior frontal gyrus (pars opercularis). Repetition deficits were associated with resection of the posterior superior temporal gyrus. Naming deficits were associated with resection of the ventral temporal cortex, with midtemporal and posterior temporal damage more predictive of naming deficits than anterior temporal damage. By 1 month postsurgery, nearly all language deficits were resolved, and no language measure except for naming differed significantly from its presurgical level.

CONCLUSIONS

These findings show that transient aphasias are very common after left hemisphere resective surgery and that the precise nature of the aphasia depends on the specific location of the surgical site. The patient cohort in this study provides a unique window into the neural basis of language because resections are discrete, their locations are not limited by vascular distribution or patterns of neurodegeneration, and language can be studied prior to substantial reorganization.

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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.