“Awake” clipping of cerebral aneurysms: report of initial series

Saleem I. Abdulrauf Departments of Neurosurgery and

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Peter Vuong Anesthesiology and

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Ritesh Patel Anesthesiology and

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Raghu Sampath Departments of Neurosurgery and

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Ahmed M. Ashour Departments of Neurosurgery and

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Lauren M. Germany Departments of Neurosurgery and

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Jonathon Lebovitz Departments of Neurosurgery and

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Colt Brunson Anesthesiology and

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Yuvraj Nijjar Anesthesiology and

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J. Kyle Dryden Anesthesiology and

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Maheen Q. Khan Departments of Neurosurgery and

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Mihaela G. Stefan Departments of Neurosurgery and

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Evan Wiley Departments of Neurosurgery and

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Ryan T. Cleary Departments of Neurosurgery and

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Connor Reis Departments of Neurosurgery and

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Jodi Walsh Saint Louis University Hospital Database,

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Paula Buchanan Saint Louis University Center for Outcomes Research, St. Louis University, Missouri

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OBJECTIVE

Risk of ischemia during aneurysm surgery is significantly related to temporary clipping time and final clipping that might incorporate a perforator. In this study, the authors attempted to assess the potential added benefit to patient outcomes of “awake” neurological testing when compared with standard neurophysiological testing performed under general anesthesia. The procedure is performed after the induction of conscious sedation, and for the neurological testing, the patient is fully awake.

METHODS

The authors conducted an institutional review board–approved prospective study of clipping unruptured intracranial aneurysms (UIAs) in 30 consecutive adult patients who underwent awake clipping. The end points were the incidence of stroke/cerebrovascular accident (CVA), death, discharge to a long-term facility, length of stay, and 30-day modified Rankin Scale score. All clinical and neurophysiological intraoperative monitoring data were recorded.

RESULTS

The median patient age was 52 years (range 27–63 years); 19 (63%) female and 11 (37%) male patients were included. Twenty-seven (90%) aneurysms were anterior, and 3 (10%) were posterior circulation aneurysms. Five (17%) had been coiled previously, 3 (10%) had been clipped previously, 2 (7%) were partially calcified, and 2 (7%) were fusiform aneurysms. Three patients developed synchronous clinical neurological and neurophysiological changes during temporary clipping with consequent removal of the temporary clip and reversal of those clinical and neurophysiological changes. Three patients developed asynchronous clinical neurological and neurophysiological changes. These 3 patients developed hemiparesis without changes in neurophysiological monitoring results. One patient developed linked clinical neurological and neurophysiological changes during final clipping that were not reversed by reapplication of the clip, and the patient had a CVA. Four patients with internal carotid artery ophthalmic segment aneurysms underwent visual testing with final clipping, and 1 of these patients required repositioning of the clip. Three patients who required permanent occlusion of a vessel as part of their aneurysm treatment underwent a 10-minute intraoperative clinical respective-vessel test occlusion. The median length of stay was 3 days (range 1–5 days). The median modified Rankin Scale score was 1 (range 0–3). All of the patients were discharged to home from the hospital except for 1 who developed a CVA and was discharged to a rehabilitation facility. There were no deaths in this series.

CONCLUSIONS

The 3 patients who developed neurological deterioration without a concomitant neurophysiological finding during temporary clipping revealed a potential advantage of awake aneurysm surgery (i.e., in decreasing the risk of ischemic injury).

ABBREVIATIONS

ACoA = anterior communicating artery; CVA = cerebrovascular accident; EEG = electroencephalography; ICA = internal carotid artery; LOS = length of stay; MCA = middle cerebral artery; MEP = motor evoked potential; mRS = modified Rankin Scale; NIS = National Inpatient Sample; SSEP = somatosensory evoked potential; UIA = unruptured intracranial aneurysm; VA = vertebral artery.

OBJECTIVE

Risk of ischemia during aneurysm surgery is significantly related to temporary clipping time and final clipping that might incorporate a perforator. In this study, the authors attempted to assess the potential added benefit to patient outcomes of “awake” neurological testing when compared with standard neurophysiological testing performed under general anesthesia. The procedure is performed after the induction of conscious sedation, and for the neurological testing, the patient is fully awake.

METHODS

The authors conducted an institutional review board–approved prospective study of clipping unruptured intracranial aneurysms (UIAs) in 30 consecutive adult patients who underwent awake clipping. The end points were the incidence of stroke/cerebrovascular accident (CVA), death, discharge to a long-term facility, length of stay, and 30-day modified Rankin Scale score. All clinical and neurophysiological intraoperative monitoring data were recorded.

RESULTS

The median patient age was 52 years (range 27–63 years); 19 (63%) female and 11 (37%) male patients were included. Twenty-seven (90%) aneurysms were anterior, and 3 (10%) were posterior circulation aneurysms. Five (17%) had been coiled previously, 3 (10%) had been clipped previously, 2 (7%) were partially calcified, and 2 (7%) were fusiform aneurysms. Three patients developed synchronous clinical neurological and neurophysiological changes during temporary clipping with consequent removal of the temporary clip and reversal of those clinical and neurophysiological changes. Three patients developed asynchronous clinical neurological and neurophysiological changes. These 3 patients developed hemiparesis without changes in neurophysiological monitoring results. One patient developed linked clinical neurological and neurophysiological changes during final clipping that were not reversed by reapplication of the clip, and the patient had a CVA. Four patients with internal carotid artery ophthalmic segment aneurysms underwent visual testing with final clipping, and 1 of these patients required repositioning of the clip. Three patients who required permanent occlusion of a vessel as part of their aneurysm treatment underwent a 10-minute intraoperative clinical respective-vessel test occlusion. The median length of stay was 3 days (range 1–5 days). The median modified Rankin Scale score was 1 (range 0–3). All of the patients were discharged to home from the hospital except for 1 who developed a CVA and was discharged to a rehabilitation facility. There were no deaths in this series.

CONCLUSIONS

The 3 patients who developed neurological deterioration without a concomitant neurophysiological finding during temporary clipping revealed a potential advantage of awake aneurysm surgery (i.e., in decreasing the risk of ischemic injury).

Awake craniotomy (defined based on 1 of 2 protocols, initiated with the patient undergoing standard mechanical ventilation and then conversion to conscious sedation for neurological testing or initiated after induction of conscious sedation and then awakening the patient for neurological testing) is not a new concept; it has widely been used for glioma resection and functional procedures for neurological monitoring of eloquent cortical and subcortical areas.7,9,10,11,12,14,16,20,21,23,25,27,29,30,32,33,34,36,37,39

Awake procedures have also been used in cerebrovascular surgery, specifically carotid endarterectomy.13,24,40 Awake craniotomy for aneurysm surgery has been presented in the literature in case report format. Lüders et al.26 reported 3 cases of distal vessel occlusion for awake testing of patients with mycotic aneurysms. Chen et al.8 reported the clipping of an ophthalmic artery aneurysm performed with the patient awake for visual testing. Passacantilli et al.31 reported trapping a giant fusiform middle cerebral artery (MCA) aneurysm with testing performed with the patient awake. Suzuki et al.35 reported the clipping of 4 aneurysms involving the anterior choroidal artery with testing performed while the patient was awake.4

During microsurgical clipping of cerebral aneurysms, the 2 steps at which patients are most at risk for neurological morbidity are as follows: 1) temporary clipping time and 2) permanent clipping of the aneurysm with an incorporated perforator(s). Despite detailed neurophysiological monitoring, morbidity and death as a result of these 2 steps are well documented in the literature. Moreover, there is essentially no established neurophysiological monitoring for temporal clipping of the basilar artery or visual function associated with clipping of ophthalmic artery aneurysms. The National (Nationwide) Inpatient Sample (NIS) has been used to deduce estimations of outcomes from clipping of unruptured intracranial aneurysms (UIAs).38 From this database, morbidity rates ranging from 13.5% to27.6% and mortality rates ranging from 0.7% to 3.5% have been reported.2,3,4,5,6,15,18,19,22,28,41

The objective of this institutional review board–approved prospective study was to assess the feasibility and efficacy of the addition of direct neurological testing during both temporary and permanent clipping of UIAs.

Methods

The standard protocol for awake craniotomy was developed and approved by the Saint Louis University institutional review board for a prospective clinical consecutive 12-month study of UIAs. The specific end points were stroke/cerebrovascular accident (CVA), discharge to a long-term facility, length of stay (LOS), 30-day modified Rankin Scale (mRS) score, and death. The mRS evaluation was performed on postoperative Day 30 (undertaken by an independent hospital-based provider specially trained in administering outcome scales). The discharge data, LOS, and mortality data were prospectively provided by the hospital information systems office. Intraoperative clinical and neurophysiological monitoring data were also collected prospectively.

The surgical procedure was performed under monitored anesthesia care. Spontaneous respirations were maintained throughout the procedure with dexmedetomidine (0.2–1.0 μg/kg per hour) and remifentanil (0.05–2 μg/kg per min) infusions. Monitoring with electroencephalography (EEG) was used to help gauge the appropriate depth of anesthesia. A scalp block with 0.5% ropivacaine was performed to anesthetize the appropriate scalp region. Before the awake phase of the surgery, the dexmedetomidine infusion was discontinued.

Intraoperative electrophysiological monitoring included EEG, somatosensory evoked potentials (SSEPs), and motor evoked potentials (MEPs). All interpretations of the electrophysiological monitoring results were made by a specially trained neurologist in the operating room.

When approaching the required neurological testing, the dexmedetomidine and remifentanil drips are halted, and the patient is brought into a fully awake stage. Intraoperative awake neurological testing included motor examination, speech examination, visual acuity testing, and field examination respective to the vascular territory tested. The visual examination was performed using the iPad-based Vision Test App 2.11 (Rocktime Ltd.).

Results

A total of 30 consecutive patients (19 female [63%] and 11 male [37%]) were included in this study. The median age was 52 years (range 27–63 years). Twenty-seven (90%) aneurysms were anterior, and 3 (10%) were posterior circulation aneurysms. Five (17%) had been coiled previously, 3 (10%) had been clipped previously, 2 (7%) were partially calcified, and 2 (6.7%) were fusiform aneurysms. More detailed patient and aneurysm features are provided in Fig. 1.

FIG. 1.
FIG. 1.

Location (A), size (B), and special features (C) of aneurysms in the study patients. ACA = anterior cerebral artery; BA = basilar artery.

Four patients were excluded during the preoperative assessment visits; 2 declined the option of awake craniotomy, and 2 were excluded by the anesthesia team during the pre-anesthesia assessment (1 because of sleep apnea and 1 because of history of difficult intubation).

All 30 patients underwent the awake-craniotomy protocol (Fig. 2). No patient needed endotracheal intubation intraoperatively or postoperatively. During dural closure, 1 patient developed an intraoperative seizure that was treated with iced saline, and the patient was kept sedated throughout the remainder of the procedure. There were no postoperative complications in this patient.

FIG. 2.
FIG. 2.

Follow-up digital subtraction angiography (DSA) performed 12 months after surgery in a 61-year-old man who underwent stent placement plus coiling of a wide-neck ICA aneurysm (at the level of the posterior communicating artery [PCoA]) revealed coil compaction. A: Anteroposterior (AP) view. B: Lateral view. The key concern in the clipping of this aneurysm was the origin of the anterior choroidal artery. C: Intraoperative photograph showing clip placement coupled with direct neurological motor examination. The patient was discharged to home on the 2nd postoperative day; he had an mRS score of 0 at the 1-month follow-up visit.

Three patients developed synchronous clinical neurological and neurophysiological findings. One patient developed contralateral hemiparesis during temporary M1 segment clipping. The temporary clip was removed immediately, and clipping of the MCA aneurysm was continued without the temporary clip. One patient developed contralateral arm weakness only during temporary M1 clipping; the temporary clip was removed immediately, and clipping of the MCA aneurysm was continued without the temporary clip. One patient developed contralateral leg weakness during the temporary clipping of the A1 segment; the temporary clip was removed immediately, and clipping of the anterior communicating artery (ACoA) aneurysm was continued without the temporary clip.

Three patients developed asynchronous (discrepant) voluntary motor-neurophysiological changes. These 3 patients developed hemiparesis without changes in neurophysiological monitoring results. One patient with a dominant A1 segment temporary clip occlusion developed immediate bilateral lower-extremity weakness without synchronous EEG or SSEP changes. No decline in the amplitudes of the MEPs was detected. The temporary clip was removed immediately, and the clipping of the ACoA aneurysm was completed without a temporary clip. No postoperative CVA was detected. One patient developed immediate contralateral hemiparesis after a temporary clip was placed on the internal carotid artery (ICA) without synchronous EEG or SSEP changes. No decline in the amplitudes of the MEPs was detected. The temporary clip was removed immediately, and clipping of the ICA aneurysm was completed without a temporary clip. No postoperative CVA was detected. One patient developed immediate contralateral arm weakness after placement of a clip on the distal M1 segment without synchronous EEG or SSEP changes. No decline in the amplitudes of the MEPs was detected (Fig. 3). The temporary clip was removed immediately, and clipping of the MCA aneurysm was completed without a temporary clip. Twenty minutes after placement of the initial temporary clip and during dural closure, a decline in the SSEPs was detected without a concomitant change in voluntary motor function. The dural closure was halted, and reinspection under a microscope followed by repeat indocyanine green angiography revealed no new changes. Results of the awake motor examination remained normal, and the SSEP changes reverted back to normal within 10 minutes. No postoperative CVA was detected.

FIG. 3.
FIG. 3.

A: 3D reconstruction of DSA images of the left ICA (AP view) in a 46-year-old man with an unruptured left MCA aneurysm. B: Intraoperative photograph showing placement of a temporary clip on distal M1 segment. C: Within seconds of placement of the temporary clip, the patient lost voluntary motor movement in his right upper extremity. D: Electrophysiological monitoring data during the loss of motor function in the right upper extremity (left column) showing SSEPs of the upper extremities (the top screen shows data from the left side, and the bottom screen shows data from the right side). The middle column shows SSEPs of the lower extremities (the top screen shows data from the left side, and the bottom screen shows data from the right side). The right column shows MEPs of the abductor pollicis brevis, adductor hallucis, and tibialis anterior of both the right and left sides. No EEG, SSEP, or MEP changes detected during the clinical motor loss were observed during the temporary clipping of the M1 segment. E: The temporary clip was removed, and the patient immediately recovered all voluntary movement of the right upper extremity. F: Final clipping was then performed without a temporary clip. The patient was discharged home on postoperative Day 3; he had an mRS score of 1 at the 1-month follow-up visit.

One patient developed linked clinical-neurophysiological changes during final clipping that were not reversed by reapplication of the clip, and the patient had developed a small capsular stroke. This patient had the longest LOS in the hospital (5 days) and was discharged to a rehabilitation institution. Thirty days after surgery, the patient had an mRS score of 3.

Four patients with an ICA aneurysm at the ophthalmic segment underwent control (precraniotomy) visual testing as the final clip was being applied. Three patients had normal (same as control) visual examination results at final awake clipping. One patient developed immediate blurring of vision in the ipsilateral eye after final clip placement. The clip was readjusted, and, within 1 minute, the patient reported resolution of the blurring and passed the iPad-based visual testing to equal control preclipping testing results. All 4 patients had normal postoperative visual examination results.

Two patients with a basilar apex aneurysm underwent level-of-consciousness testing during temporary clipping of the basilar artery. Both of them remained at the same level of consciousness as a control (just before placement of a temporary clip). The temporary clipping time was 7 minutes in the first case (Fig. 4) and 3 minutes in the second case. In both cases, multimodality (motor, speech, cranial nerve, and vision) awake testing and level-of-consciousness testing were performed during temporary clipping of the basilar artery.

FIG. 4.
FIG. 4.

A: 3D DSA image of a 45-year-old woman with a fusiform basilar apex aneurysm showing a smaller-sized left P1 segment (yellow arrow) arising from the dome of the aneurysm. B: DSA image of the left ICA showing fetal PCoA (red arrow). C: Lateral DSA image of the right ICA lateral injection showing nonfetal PCoA (red arrow). D: 3D DSA image of a basilar aneurysm with the proposed awake plan: test occlusion of the left P1 segment (yellow line) and, if passed safely, permanent occlusion of the left P1 segment and clip occlusion of the aneurysm (green line). E: Intraoperative photograph showing awake occlusion test of the left P1 segment (temporary clipping of P1). F: Screen print of the iPad-based Vision Test App 2.11, used to perform a 10-minute concomitant motor and visual examination. The patient passed the test, which was followed by permanent occlusion and cutting of the P1 segment. Next, temporary clipping of the basilar artery was performed (G), with continuous conversation with and motor examination of the patient (H). I: Finally, permanent clipping of the aneurysm was performed using 2 clips. J: Postoperative DSA image (AP view) of vertebral injection: 2 clips used for aneurysm occlusion (red arrow) and a clip occluding the left P1 segment (green arrow) are shown. K: DSA image of the left ICA (AP view) showing posterior cerebral artery territory blood flow (yellow arrow) from the left PCoA. The patient had no postoperative neurological deficits. The length of hospital stay was 3 days; her mRS score 1 month after surgery was 1.

Three patients who required permanent occlusion of a vessel as part of their aneurysm treatment underwent 10-minute intraoperative clinical respective-vessel test occlusion. After intraoperative inspection of 1 patient with a large partially calcified A1–A2 aneurysm, we felt that direct clipping was not advisable because of the high risk of embolic phenomena from the calcification. Ten-minute distal A1 segment occlusion testing was performed. No voluntary motor or electrophysiological changes were detected. Permanent occlusion was performed, and the patient did not develop a CVA postoperatively (Fig. 5). After inspection, 1 patient with a vertebral artery (VA) aneurysm was found to have more of a dissecting-type aneurysm. Ten-minute VA occlusion testing was performed. No voluntary motor, speech, cranial nerve, visual, or electrophysiological changes were detected. Permanent occlusion was performed, and the patient did not develop a CVA postoperatively. One patient with a P2–P3 fusiform aneurysm underwent a 10-minute distal P2 segment occlusion test. No voluntary motor, visual, or electrophysiological changes were detected. The patient did not develop a CVA after surgery.

FIG. 5.
FIG. 5.

Awake clip test occlusion in a 57-year-old woman who presented to an outside hospital with hydrocephalus as a result of a large partially calcified right A1–A2 junction aneurysm. A: The patient underwent placement of a ventriculoperitoneal shunt at an outside institution (axial CT image without contrast). B: DSA image of the right ICA showing slight filling of the aneurysm from the right A1 segment. C: DSA image of the left ICA revealed filling of only the left A2 segment and not the aneurysm. D: The intraoperative finding of calcifications in the right ICA and the A1 segment led us to abort the plan to perform an in situ bypass from the right A1 segment to the right A2 segment. E: Permanent occlusion of the A1 segment was considered. F: Ten minutes of temporary occlusion with a hypotensive challenge and clinical motor testing, along with neurophysiological testing (EEG, SSEPs, and MEPs), was performed. After induction of the conscious-sedation awake protocol, the patient passed intraoperative distal A1 segment occlusion testing (both clinical and neurophysiological parameters). G: Permanent occlusion of the distal A1 segment was performed. The patient was discharged home on postoperative Day 3; her mRS score 1 month after surgery was 2.

In this series (n = 30), the median LOS was 3 days (range 1–5 days). The median mRS score was 1 (range 0–3). All patients were discharged home except for one, who developed a CVA and was discharged to a rehabilitation facility. There were no deaths in this series.

Discussion

The neurosurgical concept of awake craniotomy has been well established in glioma surgery and functional procedures. Awake carotid endarterectomy, which enables neurological testing, is also well established. Aneurysm surgery involves microsurgical manipulations (temporary or permanent clipping) for specific vascular territories. Therefore, awake aneurysm microsurgery fits well with the aforementioned concept. Awake craniotomy in the treatment of aneurysms has been reported in the literature in case-report format.1,8,26,31,35 Suzuki et al.35 reported a discrepancy between MEP amplitudes and voluntary movements in 2 craniotomies performed to treat anterior choroidal artery aneurysms; in both cases, there was an immediate decline in voluntary motor movements without a concomitant change in neurophysiological monitoring after inadvertent occlusion of the anterior choroidal artery during aneurysm clipping.4

In our series (n = 30), we detected 3 (10%) patients with false-negative neurophysiological monitoring results, and all 3 developed specific respective testing deficits without concomitant neurophysiological changes while under the effects of conscious sedation. It is possible that these 3 patients would have developed a CVA if these procedures had not been performed with the awake-testing model. These initial data (n = 30) are too limited for any definitive conclusions to be made.

The conscious-sedation model for awake aneurysm surgery in this series also gave us the ability to test the feasibility of evaluating functions that we cannot routinely test after the induction of general anesthesia. Four patients underwent visual testing for the clipping of an ophthalmic segment–based aneurysm, and 2 patients with a basilar apex aneurysm underwent multimodality (consciousness level, motor, speech, cranial nerve, and vision) testing during temporary clipping of their basilar artery. We also introduced the concept of “awake clip test occlusion,” akin to the balloon test occlusion used via an endovascular technique. Three patients underwent clip test occlusion (A1 segment, VA, or P3 segment) for 10 minutes with a hypotensive challenge while we tested the respective neurological functions.

During the modern era of microsurgical clipping including neurophysiological monitoring, there has been a number of large reviews, including meta-analyses, that specifically examined the outcomes outlined in Table 1. Given the small sample (n = 30) in our study, it is not possible to make any comparisons or to draw any concrete conclusions. Larger series of awake aneurysm surgery might validate the potential benefit of this technique when compared with standard microsurgical clipping of cerebral aneurysms.

TABLE 1.

Contemporary (neurophysiological monitoring era) outcomes from clipping of UIAs

Authors & YearData Source/Study DesignNo. of PatientsLOS (days)*Discharged to a Facility (not home)No. of CVAs (%)mRS Score (median)Deaths
Barker et al., 2003NIS database/retrospective3498NA565 (16.1)NANA73 (2.1)
Barker et al., 2004NIS database/retrospective34985565 (16.1)274 (7.8)NA73 (2.1)
Higashida et al., 2007Health Economics and Outcomes Research Group of Boston Scientific Database/retrospective18817.4NA249 (13.2)NA2.50
Alshekhlee et al., 2010NIS database/retrospective37384NA340 (9)NA60 (1.6)
Hoh et al., 2010NIS/retrospective47008.9 ± 10.1NANANA
Kotowski et al., 201360 published studies, meta-analysis/retrospective9845NANA692 (7.0)NA157 (1.6)
McDonald et al., 2013Premier Inc. Perspective database/retrospective1380NA232 (17)194 (14)NA10 (0.7)
Jalbert et al., 2015Medicare provider analysis & review research identifiable files/retrospective43577.1–9.2(41.9–45.2)NANANA
Present studySingle center/prospective3031 (3)1 (3)10

NA = not applicable.

Values are median, mean ± SD, or range.

Values are number (%) or percent range.

This study was designed to be prospective. To add a framework for the outcomes of this team, we performed a retrospective review of our database to define a cohort of patients who underwent surgery for a UIA by the same neurosurgical anesthesia teams. The 2 inclusion criteria for defining the most recent retrospective computer-matched control group were aneurysm location and patient age (within 5 years). The outcome variables were exactly the same as those for the study group except for the 30-day mRS score, which was not available for the retrospective cohort. The results are shown in Table 2 (which also includes a comparison with the study-group outcomes). We provide these data purely to establish a general framework for the outcomes of patients treated by this specific team. These data show that in the LOS, discharge to a facility other than home, and risk of stroke variables, the outcomes were better for the patients who underwent awake clipping of a UIA than for those who underwent this treatment after the induction of general anesthesia. However, no definitive conclusions can be made, because the study group was prospective and the control group was retrospective.

TABLE 2.

Comparison of the outcome of the study group with a retrospective control cohort matched for aneurysm location and patient age

GroupNo. of PatientsMedian Age (yrs)Median LOS (days)No. Discharged to a Facility (not home) (%)No. of CVAs (%)mRS Score (median)No. of Deaths
Retrospective (control)305553 (10)3 (10)NA0
Prospective (study)305231 (3)1 (3)10

Conclusions

The 3 patients who developed neurological changes without a concomitant neurophysiological finding during temporary clipping revealed a potential advantage of awake aneurysm surgery in decreasing the risk of ischemic injury. In addition, this study revealed the feasibility of testing functions that are not currently testable using neurophysiological monitoring (vision, level of consciousness during temporary basilar artery clipping, and speech). The sample size (30 patients) is too small to make conclusive remarks, and additional studies are needed to study this concept further.

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Abdulrauf, Vuong, Patel, Dryden. Acquisition of data: Abdulrauf, Vuong, Patel, Sampath, Ashour, Germany, Lebovitz, Brunson, Nijjar, Dryden, Khan, Stefan, Wiley, Cleary, Reis, Walsh. Analysis and interpretation of data: Abdulrauf, Patel, Germany, Dryden, Buchanan. Drafting the article: Abdulrauf, Ashour. Critically revising the article: Abdulrauf, Khan. Reviewed submitted version of manuscript: Abdulrauf, Vuong, Patel, Sampath, Ashour, Germany, Lebovitz, Brunson, Nijjar, Dryden, Khan, Stefan, Wiley, Cleary, Reis, Buchanan. Approved the final version of the manuscript on behalf of all authors: Abdulrauf. Statistical analysis: Buchanan. Study supervision: Abdulrauf.

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    • Export Citation
  • 14

    Hervey-Jumper SL, Li J, Lau D, Molinaro AM, Perry DW, Meng L, et al.: Awake craniotomy to maximize glioma resection: methods and technical nuances over a 27-year period. J Neurosurg 123:325339, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Higashida RT, Lahue BJ, Torbey MT, Hopkins LN, Leip E, Hanley DF: Treatment of unruptured intracranial aneurysms: a nationwide assessment of effectiveness. AJNR Am J Neuroradiol 28:146151, 2007

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Hoh BL, Chi YY, Lawson MF, Mocco J, Barker FG II: Length of stay and total hospital charges of clipping versus coiling for ruptured and unruptured adult cerebral aneurysms in the Nationwide Inpatient Sample database 2002 to 2006. Stroke 41:337342, 2010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Jalbert JJ, Isaacs AJ, Kamel H, Sedrakyan A: Clipping and coiling of unruptured intracranial aneurysms among Medicare beneficiaries, 2000 to 2010. Stroke 46:24522457, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Johnston SC, Dudley RA, Gress DR, Ono L: Surgical and endovascular treatment of unruptured cerebral aneurysms at university hospitals. Neurology 52:17991805, 1999

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Johnston SC, Zhao S, Dudley RA, Berman MF, Gress DR: Treatment of unruptured cerebral aneurysms in California. Stroke 32:597605, 2001

  • 20

    Khu KJO, Bernstein M: Awake craniotomy. J Neurosurg 119:16451646, 2013. (Letter)

  • 21

    Klijn E, Hulscher HC, Balvers RK, Holland WP, Bakker J, Vincent AJ, et al.: Laser speckle imaging identification of increases in cortical microcirculatory blood flow induced by motor activity during awake craniotomy. J Neurosurg 118:280286, 2013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Kotowski M, Naggara O, Darsaut TE, Nolet S, Gevry G, Kouznetsov E, et al.: Safety and occlusion rates of surgical treatment of unruptured intracranial aneurysms: a systematic review and meta-analysis of the literature from 1990 to 2011. J Neurol Neurosurg Psychiatry 84:4248, 2013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Larkin M: Neurosurgeons wake up to awake-brain surgery. Lancet 353:1772, 1999

  • 24

    Lewis SC, Warlow CP, Bodenham AR, Colam B, Rothwell PM, Torgerson D, et al.: General anaesthesia versus local anaesthesia for carotid surgery (GALA): a multicentre, randomised controlled trial. Lancet 372:21322142, 2008

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Lucas TH II, McKhann GM II, Ojemann GA: Functional separation of languages in the bilingual brain: a comparison of electrical stimulation language mapping in 25 bilingual patients and 117 monolingual control patients. J Neurosurg 101:449457, 2004

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Lüders JC, Steinmetz MP, Mayberg MR: Awake craniotomy for microsurgical obliteration of mycotic aneurysms: technical report of three cases. Neurosurgery 56:E201, 2005

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Maldonado IL, Moritz-Gasser S, de Champfleur NM, Bertram L, Moulinié G, Duffau H: Surgery for gliomas involving the left inferior parietal lobule: new insights into the functional anatomy provided by stimulation mapping in awake patients. J Neurosurg 115:770779, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    McDonald JS, McDonald RJ, Fan J, Kallmes DF, Lanzino G, Cloft HJ: Comparative effectiveness of unruptured cerebral aneurysm therapies: propensity score analysis of clipping versus coiling. Stroke 44:988994, 2013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Meng L, Berger MS, Gelb AW: The potential benefits of awake craniotomy for brain tumor resection: an anesthesiologist's perspective. J Neurosurg Anesthesiol 27:310317, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Ogawa H, Kamada K, Kapeller C, Hiroshima S, Prueckl R, Guger C: Rapid and minimum invasive functional brain mapping by real-time visualization of high gamma activity during awake craniotomy. World Neurosurg 82:912.e1912.e10, 2014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Passacantilli E, Anichini G, Cannizzaro D, Fusco F, Pedace F, Lenzi J, et al.: Awake craniotomy for trapping a giant fusiform aneurysm of the middle cerebral artery. Surg Neurol Int 4:39, 2013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Sacko O, Lauwers-Cances V, Brauge D, Sesay M, Brenner A, Roux FE: Awake craniotomy vs surgery under general anesthesia for resection of supratentorial lesions. Neurosurgery 68:11921199, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Saito T, Muragaki Y, Maruyama T, Tamura M, Nitta M, Okada Y: Intraoperative functional mapping and monitoring during glioma surgery. Neurol Med Chir (Tokyo) 55:Suppl 1 113, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    Saito T, Tamura M, Muragaki Y, Maruyama T, Kubota Y, Fukuchi S, et al.: Intraoperative cortico-cortical evoked potentials for the evaluation of language function during brain tumor resection: initial experience with 13 cases. J Neurosurg 121:827838, 2014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Suzuki K, Mikami T, Sugino T, Wanibuchi M, Miyamoto S, Hashimoto N, et al.: Discrepancy between voluntary movement and motor-evoked potentials in evaluation of motor function during clipping of anterior circulation aneurysms. World Neurosurg 82:e739e745, 2014

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Szelényi A, Bello L, Duffau H, Fava E, Feigl GC, Galanda M, et al.: Intraoperative electrical stimulation in awake craniotomy: methodological aspects of current practice. Neurosurg Focus 28:2 E7, 2010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37

    Tate MC, Herbet G, Moritz-Gasser S, Tate JE, Duffau H: Probabilistic map of critical functional regions of the human cerebral cortex: Broca's area revisited. Brain 137:27732782, 2014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38

    Thompson BG, Brown RD Jr, Amin-Hanjani S, Broderick JP, Cockroft KM, Connolly ES Jr, et al.: Guidelines for the management of patients with unruptured intracranial aneurysms: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 46:23682400, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39

    Tuominen J, Yrjänä S, Ukkonen A, Koivukangas J: Awake craniotomy may further improve neurological outcome of intraoperative MRI-guided brain tumor surgery. Acta Neurochir (Wien) 155:18051812, 2013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    Vaniyapong T, Chongruksut W, Rerkasem K: Local versus general anaesthesia for carotid endarterectomy. Cochrane Database Syst Rev 12:CD000126, 2013

  • 41

    Zacharia BE, Ducruet AF, Hickman ZL, Grobelny BT, Badjatia N, Mayer SA, et al.: Technological advances in the management of unruptured intracranial aneurysms fail to improve outcome in New York state. Stroke 42:28442849, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Collapse
  • Expand
  • Location (A), size (B), and special features (C) of aneurysms in the study patients. ACA = anterior cerebral artery; BA = basilar artery.

  • Follow-up digital subtraction angiography (DSA) performed 12 months after surgery in a 61-year-old man who underwent stent placement plus coiling of a wide-neck ICA aneurysm (at the level of the posterior communicating artery [PCoA]) revealed coil compaction. A: Anteroposterior (AP) view. B: Lateral view. The key concern in the clipping of this aneurysm was the origin of the anterior choroidal artery. C: Intraoperative photograph showing clip placement coupled with direct neurological motor examination. The patient was discharged to home on the 2nd postoperative day; he had an mRS score of 0 at the 1-month follow-up visit.

  • A: 3D reconstruction of DSA images of the left ICA (AP view) in a 46-year-old man with an unruptured left MCA aneurysm. B: Intraoperative photograph showing placement of a temporary clip on distal M1 segment. C: Within seconds of placement of the temporary clip, the patient lost voluntary motor movement in his right upper extremity. D: Electrophysiological monitoring data during the loss of motor function in the right upper extremity (left column) showing SSEPs of the upper extremities (the top screen shows data from the left side, and the bottom screen shows data from the right side). The middle column shows SSEPs of the lower extremities (the top screen shows data from the left side, and the bottom screen shows data from the right side). The right column shows MEPs of the abductor pollicis brevis, adductor hallucis, and tibialis anterior of both the right and left sides. No EEG, SSEP, or MEP changes detected during the clinical motor loss were observed during the temporary clipping of the M1 segment. E: The temporary clip was removed, and the patient immediately recovered all voluntary movement of the right upper extremity. F: Final clipping was then performed without a temporary clip. The patient was discharged home on postoperative Day 3; he had an mRS score of 1 at the 1-month follow-up visit.

  • A: 3D DSA image of a 45-year-old woman with a fusiform basilar apex aneurysm showing a smaller-sized left P1 segment (yellow arrow) arising from the dome of the aneurysm. B: DSA image of the left ICA showing fetal PCoA (red arrow). C: Lateral DSA image of the right ICA lateral injection showing nonfetal PCoA (red arrow). D: 3D DSA image of a basilar aneurysm with the proposed awake plan: test occlusion of the left P1 segment (yellow line) and, if passed safely, permanent occlusion of the left P1 segment and clip occlusion of the aneurysm (green line). E: Intraoperative photograph showing awake occlusion test of the left P1 segment (temporary clipping of P1). F: Screen print of the iPad-based Vision Test App 2.11, used to perform a 10-minute concomitant motor and visual examination. The patient passed the test, which was followed by permanent occlusion and cutting of the P1 segment. Next, temporary clipping of the basilar artery was performed (G), with continuous conversation with and motor examination of the patient (H). I: Finally, permanent clipping of the aneurysm was performed using 2 clips. J: Postoperative DSA image (AP view) of vertebral injection: 2 clips used for aneurysm occlusion (red arrow) and a clip occluding the left P1 segment (green arrow) are shown. K: DSA image of the left ICA (AP view) showing posterior cerebral artery territory blood flow (yellow arrow) from the left PCoA. The patient had no postoperative neurological deficits. The length of hospital stay was 3 days; her mRS score 1 month after surgery was 1.

  • Awake clip test occlusion in a 57-year-old woman who presented to an outside hospital with hydrocephalus as a result of a large partially calcified right A1–A2 junction aneurysm. A: The patient underwent placement of a ventriculoperitoneal shunt at an outside institution (axial CT image without contrast). B: DSA image of the right ICA showing slight filling of the aneurysm from the right A1 segment. C: DSA image of the left ICA revealed filling of only the left A2 segment and not the aneurysm. D: The intraoperative finding of calcifications in the right ICA and the A1 segment led us to abort the plan to perform an in situ bypass from the right A1 segment to the right A2 segment. E: Permanent occlusion of the A1 segment was considered. F: Ten minutes of temporary occlusion with a hypotensive challenge and clinical motor testing, along with neurophysiological testing (EEG, SSEPs, and MEPs), was performed. After induction of the conscious-sedation awake protocol, the patient passed intraoperative distal A1 segment occlusion testing (both clinical and neurophysiological parameters). G: Permanent occlusion of the distal A1 segment was performed. The patient was discharged home on postoperative Day 3; her mRS score 1 month after surgery was 2.

  • 1

    Abdulrauf SI: Awake craniotomies for aneurysms, arteriovenous malformations, skull base tumors, high flow bypass, and brain stem lesions. J Craniovertebr Junction Spine 6:89, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Alshekhlee A, Mehta S, Edgell RC, Vora N, Feen E, Mohammadi A, et al.: Hospital mortality and complications of electively clipped or coiled unruptured intracranial aneurysm. Stroke 41:14711476, 2010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Barker FG II, Amin-Hanjani S, Butler WE, Hoh BL, Rabinov JD, Pryor JC, et al.: Age-dependent differences in short-term outcome after surgical or endovascular treatment of unruptured intracranial aneurysms in the United States, 1996–2000. Neurosurgery 54:1830, 2004

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Barker FG II, Amin-Hanjani S, Butler WE, Ogilvy CS, Carter BS: In-hospital mortality and morbidity after surgical treatment of unruptured intracranial aneurysms in the United States, 1996–2000: the effect of hospital and surgeon volume. Neurosurgery 52:9951009, 2003

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Berman MF, Solomon RA, Mayer SA, Johnston SC, Yung PP: Impact of hospital-related factors on outcome after treatment of cerebral aneurysms. Stroke 34:22002207, 2003

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Brinjikji W, Rabinstein AA, Nasr DM, Lanzino G, Kallmes DF, Cloft HJ: Better outcomes with treatment by coiling relative to clipping of unruptured intracranial aneurysms in the United States, 2001–2008. AJNR Am J Neuroradiol 32:10711075, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Chang EF, Wang DD, Perry DW, Barbaro NM, Berger MS: Homotopic organization of essential language sites in right and bilateral cerebral hemispheric dominance. J Neurosurg 114:893902, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Chen P, Dunn IF, Aglio LS, Day AL, Frerichs KU, Friedlander RM: Intraoperative awakening for vision examination during ophthalmic artery aneurysm clipping: technical case report. Neurosurgery 56:2 Suppl E440, 2005

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    De Benedictis A, Moritz-Gasser S, Duffau H: Awake mapping optimizes the extent of resection for low-grade gliomas in eloquent areas. Neurosurgery 66:10741084, 2010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    De Witte E, Satoer D, Colle H, Robert E, Visch-Brink E, Mariën P: Subcortical language and non-language mapping in awake brain surgery: the use of multimodal tests. Acta Neurochir (Wien) 157:577588, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Duffau H: The usefulness of the asleep-awake-asleep glioma surgery. Acta Neurochir (Wien) 156:14931494, 2014

  • 12

    Duffau H, Denvil D, Capelle L: Long term reshaping of language, sensory, and motor maps after glioma resection: a new parameter to integrate in the surgical strategy. J Neurol Neurosurg Psychiatry 72:511516, 2002

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Gough MJ, Bodenham A, Horrocks M, Colam B, Lewis SC, Rothwell PM, et al.: GALA: an international multicentre randomised trial comparing general anaesthesia versus local anaesthesia for carotid surgery. Trials 9:28, 2008

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Hervey-Jumper SL, Li J, Lau D, Molinaro AM, Perry DW, Meng L, et al.: Awake craniotomy to maximize glioma resection: methods and technical nuances over a 27-year period. J Neurosurg 123:325339, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Higashida RT, Lahue BJ, Torbey MT, Hopkins LN, Leip E, Hanley DF: Treatment of unruptured intracranial aneurysms: a nationwide assessment of effectiveness. AJNR Am J Neuroradiol 28:146151, 2007

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Hoh BL, Chi YY, Lawson MF, Mocco J, Barker FG II: Length of stay and total hospital charges of clipping versus coiling for ruptured and unruptured adult cerebral aneurysms in the Nationwide Inpatient Sample database 2002 to 2006. Stroke 41:337342, 2010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Jalbert JJ, Isaacs AJ, Kamel H, Sedrakyan A: Clipping and coiling of unruptured intracranial aneurysms among Medicare beneficiaries, 2000 to 2010. Stroke 46:24522457, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Johnston SC, Dudley RA, Gress DR, Ono L: Surgical and endovascular treatment of unruptured cerebral aneurysms at university hospitals. Neurology 52:17991805, 1999

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Johnston SC, Zhao S, Dudley RA, Berman MF, Gress DR: Treatment of unruptured cerebral aneurysms in California. Stroke 32:597605, 2001

  • 20

    Khu KJO, Bernstein M: Awake craniotomy. J Neurosurg 119:16451646, 2013. (Letter)

  • 21

    Klijn E, Hulscher HC, Balvers RK, Holland WP, Bakker J, Vincent AJ, et al.: Laser speckle imaging identification of increases in cortical microcirculatory blood flow induced by motor activity during awake craniotomy. J Neurosurg 118:280286, 2013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Kotowski M, Naggara O, Darsaut TE, Nolet S, Gevry G, Kouznetsov E, et al.: Safety and occlusion rates of surgical treatment of unruptured intracranial aneurysms: a systematic review and meta-analysis of the literature from 1990 to 2011. J Neurol Neurosurg Psychiatry 84:4248, 2013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Larkin M: Neurosurgeons wake up to awake-brain surgery. Lancet 353:1772, 1999

  • 24

    Lewis SC, Warlow CP, Bodenham AR, Colam B, Rothwell PM, Torgerson D, et al.: General anaesthesia versus local anaesthesia for carotid surgery (GALA): a multicentre, randomised controlled trial. Lancet 372:21322142, 2008

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Lucas TH II, McKhann GM II, Ojemann GA: Functional separation of languages in the bilingual brain: a comparison of electrical stimulation language mapping in 25 bilingual patients and 117 monolingual control patients. J Neurosurg 101:449457, 2004

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Lüders JC, Steinmetz MP, Mayberg MR: Awake craniotomy for microsurgical obliteration of mycotic aneurysms: technical report of three cases. Neurosurgery 56:E201, 2005

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Maldonado IL, Moritz-Gasser S, de Champfleur NM, Bertram L, Moulinié G, Duffau H: Surgery for gliomas involving the left inferior parietal lobule: new insights into the functional anatomy provided by stimulation mapping in awake patients. J Neurosurg 115:770779, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    McDonald JS, McDonald RJ, Fan J, Kallmes DF, Lanzino G, Cloft HJ: Comparative effectiveness of unruptured cerebral aneurysm therapies: propensity score analysis of clipping versus coiling. Stroke 44:988994, 2013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Meng L, Berger MS, Gelb AW: The potential benefits of awake craniotomy for brain tumor resection: an anesthesiologist's perspective. J Neurosurg Anesthesiol 27:310317, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Ogawa H, Kamada K, Kapeller C, Hiroshima S, Prueckl R, Guger C: Rapid and minimum invasive functional brain mapping by real-time visualization of high gamma activity during awake craniotomy. World Neurosurg 82:912.e1912.e10, 2014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Passacantilli E, Anichini G, Cannizzaro D, Fusco F, Pedace F, Lenzi J, et al.: Awake craniotomy for trapping a giant fusiform aneurysm of the middle cerebral artery. Surg Neurol Int 4:39, 2013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Sacko O, Lauwers-Cances V, Brauge D, Sesay M, Brenner A, Roux FE: Awake craniotomy vs surgery under general anesthesia for resection of supratentorial lesions. Neurosurgery 68:11921199, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Saito T, Muragaki Y, Maruyama T, Tamura M, Nitta M, Okada Y: Intraoperative functional mapping and monitoring during glioma surgery. Neurol Med Chir (Tokyo) 55:Suppl 1 113, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    Saito T, Tamura M, Muragaki Y, Maruyama T, Kubota Y, Fukuchi S, et al.: Intraoperative cortico-cortical evoked potentials for the evaluation of language function during brain tumor resection: initial experience with 13 cases. J Neurosurg 121:827838, 2014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Suzuki K, Mikami T, Sugino T, Wanibuchi M, Miyamoto S, Hashimoto N, et al.: Discrepancy between voluntary movement and motor-evoked potentials in evaluation of motor function during clipping of anterior circulation aneurysms. World Neurosurg 82:e739e745, 2014

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Szelényi A, Bello L, Duffau H, Fava E, Feigl GC, Galanda M, et al.: Intraoperative electrical stimulation in awake craniotomy: methodological aspects of current practice. Neurosurg Focus 28:2 E7, 2010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37

    Tate MC, Herbet G, Moritz-Gasser S, Tate JE, Duffau H: Probabilistic map of critical functional regions of the human cerebral cortex: Broca's area revisited. Brain 137:27732782, 2014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38

    Thompson BG, Brown RD Jr, Amin-Hanjani S, Broderick JP, Cockroft KM, Connolly ES Jr, et al.: Guidelines for the management of patients with unruptured intracranial aneurysms: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 46:23682400, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39

    Tuominen J, Yrjänä S, Ukkonen A, Koivukangas J: Awake craniotomy may further improve neurological outcome of intraoperative MRI-guided brain tumor surgery. Acta Neurochir (Wien) 155:18051812, 2013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    Vaniyapong T, Chongruksut W, Rerkasem K: Local versus general anaesthesia for carotid endarterectomy. Cochrane Database Syst Rev 12:CD000126, 2013

  • 41

    Zacharia BE, Ducruet AF, Hickman ZL, Grobelny BT, Badjatia N, Mayer SA, et al.: Technological advances in the management of unruptured intracranial aneurysms fail to improve outcome in New York state. Stroke 42:28442849, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

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