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Awake craniotomy for brain lesions within and near the primary motor area: A retrospective analysis of factors associated with worsened paresis in 102 consecutive patients

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We analyzed factors associated with worsened paresis in a large series of patients with brain lesions located within or near the primary motor area (M1) to establish protocols for safe, awake craniotomy of eloquent lesions. We studied patients with brain lesions involving M1, the premotor area (PMA) and the primary sensory area (S1), who underwent awake craniotomy (n = 102). In addition to evaluating paresis before, during, and one month after surgery, the following parameters were analyzed: Intraoperative complications; success or failure of awake surgery; tumor type (A or B), tumor location, tumor histology, tumor size, and completeness of resection. Worsened paresis at one month of follow-up was significantly associated with failure of awake surgery, intraoperative complications and worsened paresis immediately after surgery, which in turn was significantly associated with intraoperative worsening of paresis. Intraoperative worsening of paresis was significantly related to preoperative paresis, type A tumor (motor tract running in close proximity to and compressed by the tumor), tumor location within or including M1 and partial removal (PR) of the tumor. Successful awake surgery and prevention of deterioration of paresis immediately after surgery without intraoperative complications may help prevent worsening of paresis at one month. Factors associated with intraoperative worsening of paresis were preoperative motor deficit, type A and tumor location in M1, possibly leading to PR of the tumor.
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... Of course, detecting the presence of tracts does not prove these are essential to function, driving the need for intra-operative tract monitoring. However, awake surgery is not feasible in all patients, and not infallible [22]. Consequently, there is growing interest in the potential of DT not only to anticipate intra-operative findings, but-crucially-to predict post-operative functional outcomes and recovery [23][24][25][26]. ...
... We recorded similar sensitivity (84.2-100%) and specificity (85.7-100%) for 5 established surgically-relevant fiber tracts. We used more comprehensive criteria to evaluate DT, since 'gold standard' intra-operative subcortical stimulation varies in reliability and post-operative deficits can still arise [22]. When resecting tumor near eloquent tracts, some performance declines occurred without consistent stimulation findings (12 tracts, 9%). ...
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Introduction Despite evidence of correspondence with intraoperative stimulation, there remains limited data on MRI diffusion tractography (DT)’s sensitivity to predict morbidity after neurosurgical oncology treatment. Our aims were: (1) evaluate DT against subcortical stimulation mapping and performance changes during and after awake neurosurgery; (2) evaluate utility of early post-operative DT to predict recovery from post-surgical deficits. Methods We retrospectively reviewed our first 100 awake neurosurgery procedures using DT- neuronavigation. Intra-operative stimulation and performance outcomes were assessed to classify DT predictions for sensitivity and specificity calculations. Post-operative DT data, available in 51 patients, were inspected for tract damage. Results 91 adult brain tumor patients (mean 49.2 years, 43 women) underwent 100 awake surgeries with subcortical stimulation between 2014 and 2019. Sensitivity and specificity of pre-operative DT predictions were 92.2% and 69.2%, varying among tracts. Post-operative deficits occurred after 41 procedures (39%), but were prolonged (> 3 months) in only 4 patients (4%). Post-operative DT in general confirmed surgical preservation of tracts. Post-operative DT anticipated complete recovery in a patient with supplementary motor area syndrome, and indicated infarct-related damage to corticospinal fibers associated with delayed, partial recovery in a second patient. Conclusions Pre-operative DT provided very accurate predictions of the spatial location of tracts in relation to a tumor. As expected, however, the presence of a tract did not inform its functional status, resulting in variable DT specificity among individual tracts. While prolonged deficits were rare, DT in the immediate post-operative period offered additional potential to monitor neurological deficits and anticipate recovery potential.
... 10 Though a proven effective procedure for a variety of neurosurgical conditions, Awake Craniotomy is not without its drawbacks, mainly in the form of failures and postoperative complications. These have been outlined in excellent papers by Shinoura N et al., 13 and Serletis D et al. 14 ; these include worsening of paresis postoperatively or within one month of surgery, neurological deficits, intraoperative seizures (eloquently described by Nossek E et al. 15 ), postoperative hematomas requiring evacuation, and wound complications. ...
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This study aims to provide insights into the current advancements in Awake Craniotomy procedures, with a focus on Asia. Additionally, it seeks to evaluate the advantages of Awake Craniotomy over traditional methods, such as burr holes, in the treatment of brain tumors. A systematic review of available data on craniotomies is presented, with only a few exceptions. Given the scarcity of data regarding awake craniotomies in Pakistan, assumptions were made regarding the initial practices. The search encompassed all relevant articles on Awake Craniotomy and anesthesia in Awake Craniotomy.
... However, the dogma of a dominant left hemisphere and a non-dominant right hemisphere has biased the neurosurgical field towards selecting patients exclusively with left-sided lesions for awake-patient tumor resection with brain mapping [10]. The selection of patients with right-sided lesions for awake brain mapping surgery has been limited to lesions tightly related to the sensorimotor homunculus, especially in ambidextrous, or left-handed patients [6,11,12]. Nonetheless, multiple cohorts have reported long-term neurological deficits who underwent a right-sided glioma resection under general anesthesia [12][13][14], lowering the quality of life of these patients. Therefore, the goal of this systematic review is to analyze the oncological and functional outcomes after glioma resection of the right hemisphere during awake brain surgery vs resection under general anesthesia. ...
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... The second task was a sensorimotor task, in which the participants were either instructed to stay still, and the stimulation could trigger involuntary hand, leg, or eye movements. Alternatively, a motor interruption task could be performed, in which the participants were required to make a cyclic movement of their hand (as opening and closing their fingers, or moving the hand up and down) at a preferential rhythm, and the stimulation was interrupting their movement (Shinoura et al., 2013). Finally, the third possible task was a line bisection task to assess their visuospatial attention performance (Roux et al., 2011). ...
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An observer willing to cross a street must first estimate if the approaching cars offer enough time to safely complete the task. The brain areas supporting this perception, known as Time‐To‐Contact (TTC) perception, have been mainly studied through noninvasive correlational approaches. We carried out an experiment in which patients were tested during an awake brain surgery electrostimulation mapping to examine the causal implication of various brain areas in the street‐crossing decision process. Forty patients were tested in a gap acceptance task before their surgery to establish a baseline performance. The task was individually adapted upon this baseline level and carried out during their surgery. We acquired and normalized to MNI space the coordinates of the functional areas that influenced task performance. A total of 103 stimulation sites were tested, allowing to establish a large map of the areas involved in the street‐crossing decision. Multiple sites were found to impact the gap acceptance decision. A direct implication was however found mostly for sites within the right parietal lobe, while indirect implication was found for sites within the language, motor, or attentional networks. The right parietal lobe can be considered as causally influencing the gap acceptance decision. Other positive sites were all accompanied with dysfunction in other cognitive functions, and therefore should probably not be considered as the site of TTC estimation.
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Introduction: For awake craniotomy, monitored anaesthesia care (MAC) had shown relatively lower failure rates. Nevertheless, the conclusion of the appropriate anaesthetic agents, and complications, has not been proposed. Therefore, the systematic review and meta-analysis was done to compare the clinical profile, surgical outcomes, and anesthesia-related complications between dexmedetomidine-based and non-dexmedetomidine regimens during monitored anesthesia care (MAC) for this procedure. Evidence acquisition: Published clinical trials described MAC, including the amount of anaesthetic drugs, or the number of patients for awake craniotomy between January 1st, 2009 and March 31st, 2022 were reviewed through PubMed, Scopus, Google Scholar, and grey literature index. The standard methodological procedures were following the PRISMA statement with the PROSPERO registration. Twenty-two articles with 2,137 awake craniotomy patients identified as epilepsy surgery, deep brain stimulation procedure, and intracranial surgery closed to an eloquent area with intraoperative awakening for neuro-evaluation were included. The relative risk (RR) regarding surgical outcomes, and anaesthesia-related complications were compared. Evidence synthesis: Dexmedetomidine-based versus non-dexmedetomidine anaesthetic regimen revealed no statistically significant differences in surgical outcomes (RR 1.08, 95 %CI 0.94–1.24), conversion to general anaesthesia (RR 0.45, 95 %CI 0.05–3.83), respiratory complications (RR 0.4, 95 %CI 0.12–1.27), and intraoperative nausea and vomiting (RR 0.30, 95 %CI 0.08–1.14). However, the intraoperative seizure was higher in non-dexmedetomidine group (RR 4.26, 95 %CI 1.49–12.16). Conclusion: MAC for awake craniotomy with dexmedetomidine seems to be effective and safe. Randomized controlled trials with standard protocol in specific group of patients and surgical interventions would further demonstrate a clear benefit of dexmedetomidine in awake craniotomy under MAC.
Chapter
Maximal safe resection of gliomas and preserving eloquent areas is the aim of surgery. In epilepsy surgery, the goal is resection of the epileptogenic zone to control epilepsy while preserving function. To identify the epileptogenic zone electrophysiological and neuroradiological studies should be done. Non-invasive studies, such as magnetic resonance imaging (MRI) and magnetoencephalography (MEG) have progressed markedly [1, 2]; whereas, identification of epileptogenic zones requires invasive evaluation. Epileptogenic foci such as focal cortical dysplasia (FCD) type 1 often show minimal histopathological and imaging changes. These foci are often located in eloquent areas requiring awake surgery.
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CNS invasion has been included as an independent criterion for the diagnosis of a high-grade (WHO and CNS grade 2 and 3) meningioma in the 2016 and more recently in the 2021 WHO classification. However, the prognostic role of brain invasion has recently been questioned. Also, surgical treatment for brain invasive meningiomas may pose specific challenges. We conducted a systematic review of the 2016–2022 literature on brain invasive meningiomas in Pubmed, Scopus, Web of Science and the Cochrane Library. The prognostic relevance of brain invasion as a stand-alone criterion is still unclear. Additional and larger studies using robust definitions of histological brain invasion and addressing the issue of sampling errors are clearly warranted. Although the necessity of molecular profiling in meningioma grading, prognostication and decision making in the future is obvious, specific markers for brain invasion are lacking for the time being. Advanced neuroimaging may predict CNS invasion preoperatively. The extent of resection (e.g., the Simpson grading) is an important predictor of tumor recurrence especially in higher grade meningiomas, but also – although likely to a lesser degree – in benign tumors, and therefore also in brain invasive meningiomas with and without other histological features of atypia or malignancy. Hence, surgery for brain invasive meningiomas should follow the principles of maximal but safe resections. There are some data to suggest that safety and functional outcomes in such cases may benefit from the armamentarium of surgical adjuncts commonly used for surgery of eloquent gliomas such as intraoperative monitoring, awake craniotomy, DTI tractography and further advanced intraoperative brain tumor visualization.
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Background For patients undergoing brain surgery, once primary motor and sensory areas are identified by direct electrical stimulation (DES), resection can be performed in the pre-central and post-somatosensory areas while monitoring cognition. For this purpose, we developed a real-time neuropsychological testing (RTNT) protocol tapping sensorimotor cognition. Methods We retrospectively reviewed a consecutive series of 57 adult patients with tumors in the pre-central and post-somatosensory areas who performed the RTNT sequence. The testing protocol used continuously throughout resection for excisions comprised action verbs, mental rotation of body parts, action imagery, action semantics, ideomotor praxis and short-term memory. Results The patients’ median performance on RTNT tests was significantly lower for mental rotation and action imagery (χ²(2) = 55.98, p < 0.001), as well as their minimum value of patients’ performance (χ²(2) = 85.048, p < 0.001) and their delta calculated between the patients’ performance at the first vs the last RTNT run (χ²(2) = 14.33, p < 0.05). Patients showing such decreases in performance on action imagery had lesions overlapping on the right pre- and post-central gyrus, the SMA, and the superior and inferior parietal lobe. For the mental rotation task, their maximum lesion overlay included the right cingulum/SMA and left superior and inferior parietal lobe and medial precuneus. The mean resection extent was 91.15% ±17.45 and correlated with the number of motor-related positive sites DES at cortical (r=-.279, p=.020) and white matter (r=-.417, p=.001) level. Conclusions The sensory-motor RTNT is performed to assist surgery in the pre-central and post-somatosensory areas.
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Introduction Awake craniotomy (AC) has emerged as a better modality for resection of intra-axial brain tumors. The advantages are not just related to the preservation of neurological function, but also include early recovery, short hospital stay and possibly lower costs. However, data on AC for meningioma resection is deficient, likely because of concerns related to intra-operative pain and blood loss. Methods All patients who underwent AC, using awake through-out technique for resection of meningioma, during the last five years, were included in the study. Non-probability consecutive sampling technique was employed. Variables for demographics, and details of diagnosis and surgical procedure were recorded. The outcomes measured were length of hospital stay, worsening of neurological function during surgery and significant intra-operative or post-operative pain. Results Seventeen patients underwent AC for resection of meningioma during the study period. Eleven of these were grade I meningioma, and six were grade II meningioma. The mean age was 45.8 ± 10.5 years. Presenting complaints were variable, with seizures being the most common (n = 7; 41.2%). The mean duration of surgery was 180.8 ± 36.2 minutes and median estimated blood loss was 450 ml (IQR: 225 ml - 737.5 ml). The mean length of stay in the hospital was 3.1 ± 1.3 days. Only one patient had a prolonged hospital stay of seven days, because of post-operative seizures. Eleven patients (58.3%) had convexity meningioma, 4 (33.3%) had parasagittal meningioma and 1 each had a parafalcine and anterior skull-base meningioma. Simpson grade I resection was performed in 6 (41.7%) patients, grade II resection in 10 (50%) patients, and grade III resection in 1 (5.9%) patient. None of our patients had deterioration in their neurological deficits after surgery and no one required emergency intubation, conversion of surgery to general anesthesia, or redo exploration. Conclusion AC may be considered a safe modality for surgical resection of convexity and parasagittal meningioma, with no significant risk of intra-operative or post-operative pain, although it requires more evidence. It can be offered to patients who are at higher risk, or are not willing to undergo general anesthesia. Ultimately, it might also be beneficial in terms of reducing overall costs.
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Glioma resection under conscious ("awake") sedation (CS) is used for eloquent areas of the brain to minimize postoperative neurological deficits. The objective of this study was to compare the duration of hospital stay, overall hospital cost, perioperative morbidity, and postoperative patient functional status in patients whose gliomas were resected using CS versus general endotracheal anesthesia (GEA). Twenty-two cases in 20 patients who underwent surgery for cerebral gliomas under CS and a matched cohort of 22 cases in 19 patients who underwent surgery under GEA over a 3-year period were retrospectively evaluated. Criteria for inclusion in the study were as follows: 1) a single cerebral lesion; 2) gross-total resection as evidenced by postoperative Gd-enhanced MR imaging within 48 hours of surgery; 3) a WHO Grade II, III, or IV glioma; 4) a supratentorial lesion location; 5) a Karnofsky Performance Scale score ≥ 70; 6) an operation performed by the same neurosurgeon; and 7) an elective procedure. The average hospital stay was significantly different between the 2 groups: 3.5 days for patients who underwent CS and 4.6 days for those who underwent GEA. This result translated into a significant decrease in the average inpatient cost after intensive care unit (ICU) care for the CS group compared with the GEA group. Other variables were not significantly different. Patients undergoing glioma resection using CS techniques have a significantly shorter hospital stay with reduced inpatient hospital expenses after postoperative ICU care.
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Objective: An awake craniotomy facilitates radical excision of eloquent area gliomas and ensures neural integrity during the excision. The study describes our experience with 67 consecutive awake craniotomies for the excision of such tumours. Methods: Sixty-seven patients with gliomas in or adjacent to eloquent areas were included in this study. The patient was awake during the procedure and intraoperative cortical and white matter stimulation was performed to safely maximize the extent of surgical resection. Results: Of the 883 patients who underwent craniotomies for supratentorial intraaxial tumours during the study period, 84 were chosen for an awake craniotomy. Sixty-seven with a histological diagnosis of glioma were included in this study. There were 55 men and 12 women with a median age of 34.6 years. Forty-two (62.6%) patients had positive localization on cortical stimulation. In 6 (8.9%) patients white matter stimulation was positive, five of whom had responses at the end of a radical excision. In 3 patients who developed a neurological deficit during tumour removal, white matter stimulation was negative and cessation of the surgery did not result in neurological improvement. Sixteen patients (24.6%) had intraoperative neurological deficits at the time of wound closure, 9 (13.4%) of whom had persistent mild neurological deficits at discharge, while the remaining 7 improved to normal. At a mean follow-up of 40.8 months, only 4 (5.9%) of these 9 patients had persistent neurological deficits. Conclusion: Awake craniotomy for excision of eloquent area gliomas enable accurate mapping of motor and language areas as well as continuous neurological monitoring during tumour removal. Furthermore, positive responses on white matter stimulation indicate close proximity of eloquent cortex and projection fibres. This should alert the surgeon to the possibility of postoperative deficits to change the surgical strategy. Thus the surgeon can resect tumour safely, with the knowledge that he has not damaged neurological function up to that point in time thus maximizing the tumour resection and minimizing neurological deficits.
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Object: Awake craniotomy for removal of intraaxial tumors within or adjacent to eloquent brain regions is a well-established procedure. However, awake craniotomy failures have not been well characterized. In the present study, the authors aimed to analyze and assess the incidence and causes for failed awake craniotomy. Methods: The database of awake craniotomies performed at Tel Aviv Medical Center between 2003 and 2010 was reviewed. Awake craniotomy was considered a failure if conversion to general anesthesia was required, or if adequate mapping or monitoring could not have been achieved. Results: Of 488 patients undergoing awake craniotomy, 424 were identified as having complete medical, operative, and anesthesiology records. The awake craniotomies performed in 27 (6.4%) of these 424 patients were considered failures. The main causes of failure were lack of intraoperative communication with the patient (n = 18 [4.2%]) and/or intraoperative seizures (n = 9 [2.1%]). Preoperative mixed dysphasia (p < 0.001) and treatment with phenytoin (p = 0.0019) were related to failure due to lack of communication. History of seizures (p = 0.03) and treatment with multiple antiepileptic drugs (p = 0.0012) were found to be related to failure due to intraoperative seizures. Compared with the successful awake craniotomy group, a significantly lower rate of gross-total resection was achieved (83% vs 54%, p = 0.008), there was a higher incidence of short-term speech deterioration postoperatively (6.1% vs 23.5%, p = 0.0017) as well as at 3 months postoperatively (2.3% vs 15.4%, p = 0.0002), and the hospitalization period was longer (4.9 ± 6.2 days vs 8.0 ± 10.1 days, p < 0.001). Significantly more major complications occurred in the failure group (4 [14.8%] of 27) than in the successful group (16 [4%] of 397) (p = 0.037). Conclusions: Failures of awake craniotomy were associated with a lower incidence of gross-total resection and increased postoperative morbidity. The majority of awake craniotomy failures were preventable by adequate patient selection and avoiding side effects of drugs administered during surgery.
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The use of an awake craniotomy in the treatment of supratentorial lesions is a challenge for both patients and staff in the operation theater. To assess the safety and effectiveness of an awake craniotomy with brain mapping in comparison with a craniotomy performed under general anesthesia. We prospectively compared 2 groups of patients who underwent surgery for supratentorial lesions: those in whom an awake craniotomy with intraoperative brain mapping was used (AC group, n = 214) and those in whom surgery was performed under general anesthesia (GA group, n = 361, including 72 patients with lesions in eloquent areas). The AC group included lesions in close proximity to the eloquent cortex that were surgically treated on an elective basis. Globally, the 2 groups were comparable in terms of sex, age, American Society of Anesthesiologists score, pathology, size of lesions, quality of resection, duration of surgery, and neurological outcome, and different in tumor location and preoperative neurological deficits (higher in the AC group). However, specific data analysis of patients with lesions in eloquent areas revealed a significantly better neurological outcome and quality of resection (P < .001) in the AC group than the subgroup of GA patients with lesions in eloquent areas. Surgery was uneventful in AC patients and they were discharged home sooner. AC with brain mapping is safe and allows maximal removal of lesions close to functional areas with low neurological complication rates. It provides an excellent alternative to craniotomy under GA.
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Patients undergoing awake surgery for resection of brain tumours in the primary motor cortex (M1) are at high risk of developing new motor deficits. Thus, use of this procedure requires consideration of several important points, including the optimal modality to localise M1 on the affected side and the overall advantages and disadvantages of the procedure. In our experience with awake surgery for 21 brain tumours located in the M1 from January 2004 through October 2008, we found that functional magnetic resonance imaging was the most reliable modality in terms of localising the M1 and that the anatomic relationship between motor tracts and brain tumours is a critical determinant of postoperative motor function. Other considerations, including potential complications of this procedure and relative efficacy and safety versus surgery under general anaesthesia for patients with brain tumours in the M1, are discussed.
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Localization of brain function is a fundamental requisite for the resection of eloquent-area brain tumors. Preoperative functional neuroimaging and diffusion tensor imaging can display cortical functional organization and subcortical anatomy of major white matter bundles. Direct cortical and subcortical stimulation is widely used in routine practice, however, because of its ability to reveal tissue function in eloquent regions. The role and integration of these techniques is still a matter of debate. The objective of this study was to assess surgical and functional neurological outputs of awake surgery and intraoperative cortical and subcortical electrical stimulation (CSES) and to use CSES to examine the reliability of preoperative functional magnetic resonance (fMRI) and diffusion tensor imaging fiber tracking (DTI-FT) for surgical planning. We prospectively studied 27 patients with eloquent-area tumors who were selected to undergo awake surgery and direct brain mapping. All subjects underwent preoperative sensorimotor and language fMRI and DTI tractography of major white matter bundles. Intra- and postoperative complications, stimulation effects, extent of resection, and neurological outcome were determined. We topographically correlated intraoperatively identified sites (cortical and subcortical) with areas of fMRI activation and DTI tractography. Total plus subtotal resection reached 88.8%. Twenty-one patients (77.7%) suffered transient postoperative worsening, but at 6 months follow-up only three (11.1%) patients had persistent neurological impairment. Sensorimotor cortex direct mapping correlated 92.3% with fMRI activation, while direct mapping of language cortex correlated 42.8%. DTI fiber tracking underestimated the presence of functional fibers surrounding or inside the tumor. Preoperative brain mapping is useful when planning awake surgery to estimate the relationship between the tumor and functional brain regions. However, these techniques cannot directly lead the surgeon during resection. Intraoperative brain mapping is necessary for safe and maximal resection and to guarantee a satisfying neurological outcome. This multimodal approach is more aggressive, leads to better outcomes, and should be used routinely for resection of lesions in eloquent brain regions.
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Awake craniotomy with intraoperative electrical mapping is a reliable method to minimize the risk of permanent deficit during surgery for low-grade glioma located within eloquent areas classically considered inoperable. However, it could be argued that preservation of functional sites might lead to a lesser degree of tumor removal. To the best of our knowledge, the extent of resection has never been directly compared between traditional and awake procedures. We report for the first time a series of patients who underwent 2 consecutive surgeries without and with awake mapping. Nine patients underwent surgery for a low-grade glioma in functional sites under general anesthesia in other institutions. The resection was subtotal in 3 cases and partial in 6 cases. There was a postoperative worsening in 3 cases. We performed a second surgery in the awake condition with intraoperative electrostimulation. The resection was performed according to functional boundaries at both the cortical and subcortical levels. Postoperative magnetic resonance imaging showed that the resection was complete in 5 cases and subtotal in 4 cases (no partial removal) and that it was improved in all cases compared with the first surgery (P = .04). There was no permanent neurological worsening. Three patients improved compared with the presurgical status. All patients returned to normal professional and social lives. Our results demonstrate that awake surgery, known to preserve the quality of life in patients with low-grade glioma, is also able to significantly improve the extent of resection for lesions located in functional regions.