Update: Awake surgery

An awake craniotomy is a safe neurosurgical procedure that minimizes the risk of brain injury. During the course of this surgery, the patient is asked to perform motor or cognitive tasks, but some patients exhibit severe sleepiness.

For neurosurgery with an awake craniotomy, the critical issue is to set aside enough time to identify eloquentcortices by electrocortical stimulation (ECS). High gamma activity (HGA) ranging between 80 and 120 Hz on electrocorticogram (ECoG) is assumed to reflect localized cortical processing.

Indications

Gross total removal of glioma is limited by proximity to eloquent brain. Awake surgery allows for intraoperative monitoring to safely identify eloquent regions.


For a long time, the right hemisphere (RH) was considered as “non-dominant”, especially in right-handers. In neurosurgical practice, this dogma resulted in the selection of awake craniotomy with language mapping only for lesions of the left dominant hemisphere. Conversely, surgery under general anesthesia (possibly with motor mapping) was usually proposed for right lesions. However, when objective neuropsychological tests were performed, they frequently revealed cognitive and behavioral deficits following brain surgery, even in the RH. Therefore, to preserve an optimal quality of life, especially in patients with a long survival expectancy (as in low-grade gliomas), awake surgery with cortical and axonal electrostimulation mapping has recently been proposed for right tumors resection. Here, we review new insights gained from intraoperative stimulation into the pivotal role of the RH in movement execution and control, visual processes and spatial cognition, language and non-verbal semantic processing, executive functions (e.g. attention), and social cognition (mentalizing and emotion recognition). Such original findings, that break with the myth of a “non-dominant” RH, may have important implications in cognitive neurosciences, by improving our knowledge of the functional connectivity of the RH, as well as for the clinical management of patients with a right lesion. Indeed, in brain surgery, awake mapping should be considered more systematically in the RH. Moreover, neuropsychological examination must be achieved in a more systematic manner before and after surgery within the RH, to optimize the care by predicting the likelihood of functional recovery and by elaborating specific programs of rehabilitation 1).

Operations in eloquent areas

Awake craniotomy was introduced for surgical treatment of epilepsy, and has subsequently been used in patients with supratentorial tumors, intracranial arteriovenous malformationdeep brain stimulation, and mycotic aneurysms near critical regions of brain.

Patients are selected for awake craniotomy when the planned procedure involves eloquent areas of the brain, necessitating an awake, cooperative patient capable of undergoing neurocognitive testing, especially speech area, (Broca’s areaWernicke’s area) near motor stripthalamus, removal of brainstem tumors, some seizure surgery.

The critical issue is to set aside enough time to identify eloquent cortices by electrocortical stimulation (ECS). High gamma activity (HGA) ranging between 80 and 120 Hz on electrocorticogram (ECoG) is assumed to reflect localized cortical processing. In this report, we used realtime HGA mapping and functional magnetic resonance imaging (fMRI) for rapid and reliable identification of motor and language functions. Three patients with intra-axial tumors in their dominant hemisphere underwent preoperative fMRI and lesion resection with an awake craniotomy. All patients showed significant fMRI activation evoked by motor and language tasks. After the craniotomy, we recorded ECoG activity by placing subdural grids directly on the exposed brain surface. Each patient performed motor and language tasks and demonstrated realtime HGA dynamics in hand motor areas and parts of the inferior frontal gyrus. Sensitivity and specificity of HGA mapping were 100% compared to ECS mapping in the frontal lobe, which suggested HGA mapping precisely indicated eloquent cortices. The investigation times of HGA mapping was significantly shorter than that of ECS mapping. Specificities of the motor and language-fMRI, however, did not reach 85%. The results of HGA mapping was mostly consistent with those of ECS mapping, although fMRI tended to overestimate functional areas. This novel technique enables rapid and accurate functional mapping 2).

Awake craniotomy for glioma

Craniotomies for glioma resection under conscious sedation (CS) have been well-documented in the literature for gliomas that are in or adjacent to eloquent areas 3) 4) 5) 6) 7).

Awake surgery for glioma aims to maximize resection to optimize prognosis while minimizing the risk of postoperative deficits.

The oncological and functional results of awake glioma surgery during the learning curve are comparable to results from established centers. The use and utility of resection probability maps are well demonstrated. The return to work level is high 8).

AC with the input of the speech and language therapist (SLT) and an experienced neuro-physiotherapist (NP) is a key component in ensuring optimal functional outcomes for patients with gliomas in eloquently located areas 9).

5 aminolevulinic acid guidance during awake craniotomy

Corns et al. describe the case of a patient with recurrent left frontal GBM encroaching on Broca’s area (eloquent brain). Gross total resection of the tumour was achieved by combining two techniques, awake resection to prevent damage to eloquent brain and 5-ALA fluorescence guidance to maximise the extent of tumour resection.This technique led to gross total resection of all T1-enhancing tumour with the avoidance of neurological deficit. The authors recommend this technique in patients when awake surgery can be tolerated and gross total resection is the aim of surgery 10)

Contraindications

Uncooperative (very young or too old patient).

Confusion.

Speech deficit

Language barrier

Brain mapping

Electrocortical stimulation (ECS) is the gold standard for functional brain mapping during an awake craniotomy.

Awake craniotomy could be challenging because of unsecured airway with risks of vomitting, epileptic attacks or unstable level of consciousness. It is considered that the patient monitoring becomes more difficult when iMRI is performed because the patient’s face cannot be obsereved directly. We should remember that conscious level as well as respiration pattern may change during operation 11).

Awake craniotomy can be safely performed in a high-field (1.5 T) iMRI suite to maximize tumor resection in eloquent brain areas with an acceptable morbidity profile at 1 month 12).

The routine use of fMRI was not useful in identifying language sites as performed and, more importantly, practiced tasks failed to prevent neurological deficits following awake craniotomy procedures 13).

Management of anesthesia

The importance of minimizing pain and preparing patients thoroughly to reduce anxiety and maximize cooperation. Awake surgery is an excellent treatment modality for brain tumors with very positive perception by patients 14).

Different anesthetic combinations, including neurolept, propofol with or without opioid infusions, and asleep-awake-asleep techniques, have been reported for awake craniotomy. In all these techniques, respiratory depression has been reported as a complication.

see dexmedetomidine

Different protocols exist for anesthetic care during awake craniotomy based on monitored anesthesia care (MAC) or general anesthesia (asleep-awake-asleep technique). Nevertheless the administration of anesthetics, expectedly, is not without drawbacks, side effects and risks. A new approach for awake craniotomies emphasizes the need of adequate communication with patients 15).

Scalp block

see http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4236942/#ref11

Awake surgery with intraoperative brain mapping is highly recommended for patients with diffuse low grade gliomas in language areas, to maximise the extent of resection while preserving the integrity of functional networks and thus quality of life.

The picture naming test DO 80 is the gold standard for language assessment before, during, and after surgery.

Cognitive functioning is correlated with quality of life, itself linked with return to work.

The objective was to evaluate the significance of measuring naming speed, and its correlation with the return to professional activities. Two complementary studies are reported. In the first retrospective study, eleven patients were examined post-operatively. Five patients were selected because they were not able to resume their professional activities (“no return group 1”). They were compared with a control group of six patients who are working normally after surgery (“return group 1”). The eleven patients performed a global language and neuropsychological assessment, with a post-operative median follow-up of 35 months. In a subsequent prospective study, twelve patients were examined pre-operatively and post-operatively. Six patients who were not able to return to work (“no return group 2”) were compared with a control group of six patients who were working normally after the surgery (“return group 2”). The twelve patients performed a pre and post-operative language assessment, with a median follow-up of 9 months. Our results show, for the first time, that naming speed is significantly correlated with a major criterion of quality of life: the return to professional activities. There were no differences between the two groups regarding other measures of cognition. Assessing naming times, and not only naming accuracy, is essential in the management of low-grade glioma patients, before, during, and after surgery, to preserve their quality of life by resuming their previous professional activity. Our results have fundamental implications concerning the comprehension of language processing and its relationship with cognitive functioning 16).

Cost effectiveness

Retrospective analysis of a cohort of 17 patients with perirolandic gliomas who underwent an AC with DCS were case-control matched with 23 patients with perirolandic gliomas who underwent surgery under GA with neuromonitoring (ie, motor-evoked potentials, somatosensory-evoked potentials, phase reversal). Inpatient costs, quality-adjusted life years (QALY), extent of resection, and neurological outcome were compared between the groups.

Total inpatient expense per patient was ${\$}$ 34 804 in the AC group and ${\$}$ 46 798 in the GA group ( P = .046). QALY score for the AC group was 0.97 and 0.47 for the GA group ( P = .041). The incremental cost per QALY for the AC group was ${\$}$ 82 720 less than the GA group. Postoperative Karnofsky performance status was 91.8 in the AC group and 81.3 in the GA group (P = .047). Length of hospitalization was 4.12 days in the AC group and 7.61 days in the GA group ( P = .049).

The total inpatient costs for awake craniotomies were lower than surgery under GA. This study suggests better cost effectiveness and neurological outcome with awake craniotomies for perirolandic gliomas 17).

Case series

2017

Motomura et al. retrospectively reviewed the records of 33 consecutive patients with glial tumors in the eloquent brain areas who underwent awake surgery using iMRI. Volumetric analysis of MRI studies was performed. The pre-, intra-, and postoperative tumor volumes were measured in all cases using MRI studies obtained before, during, and after tumor resection. RESULTS Intraoperative MRI was performed to check for the presence of residual tumor during awake surgery in a total of 25 patients. Initial iMRI confirmed no further tumor resection in 9 patients (36%) because all observable tumors had already been removed. In contrast, intraoperative confirmation of residual tumor during awake surgery led to further tumor resection in 16 cases (64%) and eventually an EOR of more than 90% in 8 of 16 cases (50%). Furthermore, EOR benefiting from iMRI by more than 15% was found in 7 of 16 cases (43.8%). Interestingly, the increase in EOR as a result of iMRI for tumors associated mainly with the insular lobe was significantly greater, at 15.1%, than it was for the other tumors, which was 8.0% (p = 0.001).

This study revealed that combining awake surgery with iMRI was associated with a favorable surgical outcome for intrinsic brain tumors associated with eloquent areas. In particular, these benefits were noted for patients with tumors with complex anatomy, such as those associated with the insular lobe 18).

2016

Four illustrative cases demonstrate the efficacy of using a tablet computer platform for advanced language mapping testing with sophisticated language paradigms, and the spatial agreement between intraoperative mapping and preoperative fMRI results. The testing platform substantially improved the ability of the surgeon to detect and characterize language deficits. Use of a written word generation task to assess language production helped confirm areas of speech apraxia and speech arrest that were inadequately characterized or missed with the use of traditional paradigms, respectively. Preoperative fMRI of the analogous writing task was also assistive, displaying excellent spatial agreement with intraoperative mapping in all 4 cases. Sole use of traditional testing paradigms can be limiting during awake craniotomy procedures. Comprehensive assessment of language function will require additional use of more sophisticated and ecologically valid testing paradigms. The platform presented here provides a means to do so 19).

2015

Thirty-seven patients with brain tumor who underwent awake craniotomy were included in this study. Prior to craniotomy, the patient evaluated cognitive status, and during the surgery, each patient’s performance and attitude toward cognitive tasks were recorded by neuropsychologists.

The present findings showed that the construction and calculation abilities of the patients were moderately correlated with their sleepiness.

These results indicate that the preoperative cognitive functioning of patients was related to their sleepiness during the awake craniotomy procedure and that the patients who exhibited sleepiness during an awake craniotomy had previously experienced reduced functioning in the parietal lobe 20).

2009

From 1998 to 2007, 79 consecutive fully awake craniotomy (FAC)s for resection primary supratentorial brain tumors (PSBT) near or in eloquent brain areas (EBA), performed by a single surgeon, were prospectively followed. Two groups were defined based on time period and surgical team: group A operated on from March 1998 to July 2004 without a multidisciplinary team and group B operated on from August 2004 to October 2007 in a multidisciplinary setting. For both time periods, two groups were defined: group I had no previous history of craniotomy, while group II had undergone a previous craniotomy for a PSBT. Forty-six patients were operated on in group A, 46 in group B, 49 in group I and 30 in group II. Psychological assessment and selection were obligatory. The preferred anesthetic procedure was an intravenous high-dose opioid infusion (Fentanil 50 microg, bolus infusion until a minimum dose of 10 microg/kg). Generous scalp and periosteous infiltrations were performed. Functional cortical mapping was performed in every case. Continuous somato-sensory evoked potentials (SSEPs) and phase reversal localization were available in 48 cases. Standard microsurgical techniques were performed and monitored by continuous clinical evaluation.

Clinical data showed differences in time since clinical onset (p < 0.001), slowness of thought (p = 0.02) and memory deficits (p < 0.001) between study periods and also time since recent seizure onset for groups I and II (p = 0.001). Mean tumor volume was 51.2 +/- 48.7 cm3 and was not different among the four groups. The mean extent of tumor reduction was 90.0 +/- 12.7% and was similar for the whole series. A trend toward a larger incidence of glioblastoma multiforme occurred in group B (p = 0.05) and I (p = 0.04). Recovery of previous motor deficits was observed in 75.0% of patients, while motor worsening in 8.9% of cases. Recovery of semantic language deficits, control of refractory seizures and motor worsening were statistically more frequent in group B (p = 0.01). Satisfaction with the procedure was reported by 89.9% of patients, which was similar for all groups. Clinical complications were minimal, and surgical mortality was 1.3%.

These data suggest that FAC is safe and effective for the resection of PSBT in EBA as the main technique, and in a multidisciplinary context is associated with greater clinical and physiological monitoring. The previous history of craniotomy for PSBT did not seem to influence the outcome21).

1)

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Kamada K, Ogawa H, Kapeller C, Prueckl R, Guger C. Rapid and low-invasive functional brain mapping by realtime visualization of high gamma activity for awake craniotomy. Conf Proc IEEE Eng Med Biol Soc. 2014 Aug;2014:6802-6805. PubMed PMID: 25571558.

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De Benedictis A, Mortiz-Gasser S, Duffau H. Awake mapping optimizes the extent of resection for low-grade gliomas in eloquent areas. Neurosurgery 2010;66:1074-84.

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Peruzzi P, Bergese SD, Viloria A, Puente EG, Abdel-Rasoul M, Chiocca EA. A retrospective cohort-matched comparison of conscious sedation versus general anesthesia for supratentorial glioma resection. Clinical article. J Neurosurg 2011;114:633-9.

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Taylor MD, Bernstein M. Awake craniotomy with brain mapping as the routine surgical approach to treating patients with supratentorial intraaxial tumors: A prospective trial of 200 cases. J Neurosurg 1999;90:35-41.

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Wiedemayer H, Sandalcioglu IE, Armbruster W, Regel J, Schaefer H, Stolke D. False negative findings in intraoperative SEP monitoring: Analysis of 658 consecutive neurosurgical cases and review of published reports. J Neurol Neurosurg Psychiatry 2004;75:280-6.

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Mandonnet E, De Witt Hamer P, Poisson I, Whittle I, Bernat AL, Bresson D, Madadaki C, Bouazza S, Ursu R, Carpentier AF, George B, Froelich S. Initial experience using awake surgery for glioma: oncological, functional, and employment outcomes in a consecutive series of 25 cases. Neurosurgery. 2015 Apr;76(4):382-9. doi: 10.1227/NEU.0000000000000644. PubMed PMID: 25621981.

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Trimble G, McStravick C, Farling P, Megaw K, McKinstry S, Smyth G, Law G, Courtney H, Quigley G, Flannery T. Awake craniotomy for glioma resection: Technical aspects and initial results in a single institution. Br J Neurosurg. 2015 Jul 13:1-7. [Epub ahead of print] PubMed PMID: 26168299.

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Corns R, Mukherjee S, Johansen A, Sivakumar G. 5-aminolevulinic acid guidance during awake craniotomy to maximise extent of safe resection of glioblastoma multiforme. BMJ Case Rep. 2015 Jul 15;2015. pii: bcr2014208575. doi: 10.1136/bcr-2014-208575. PubMed PMID: 26177997.

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Kamata K, Wada K, Kinoshita M, Nomura M, Ozaki M. [A case of respiratory arrest during intraoperative magnetic resonance imaging (iMRI) for awake craniotomy]. Masui. 2014 Aug;63(8):907-10. Japanese. PubMed PMID: 25199330.

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Maldaun MV, Khawja SN, Levine NB, Rao G, Lang FF, Weinberg JS, Tummala S, Cowles CE, Ferson D, Nguyen AT, Sawaya R, Suki D, Prabhu SS. Awake craniotomy for gliomas in a high-field intraoperative magnetic resonance imaging suite: analysis of 42 cases. J Neurosurg. 2014 Oct;121(4):810-7. doi: 10.3171/2014.6.JNS132285.Epub 2014 Aug 8. PubMed PMID: 25105702.

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Trinh VT, Fahim DK, Maldaun MV, Shah K, McCutcheon IE, Rao G, Lang F, Weinberg J, Sawaya R, Suki D, Prabhu SS. Impact of Preoperative Functional Magnetic Resonance Imaging during Awake Craniotomy Procedures for Intraoperative Guidance and Complication Avoidance. Stereotact Funct Neurosurg. 2014 Sep 18;92(5):315-322. [Epub ahead of print] PubMed PMID: 25247627.

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Hansen E, Seemann M, Zech N, Doenitz C, Luerding R, Brawanski A. Awake craniotomies without any sedation: The awake-awake-awake technique. Acta Neurochir (Wien) 2013;155:1417–24.

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Moritz-Gasser S, Herbet G, Maldonado IL, Duffau H. Lexical access speed is significantly correlated with the return to professional activities after awake surgery for low-grade gliomas. J Neurooncol. 2012 May;107(3):633-41. doi: 10.1007/s11060-011-0789-9. Epub 2012 Jan 24. PubMed PMID: 22270847.

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Eseonu CI, Rincon-Torroella J, ReFaey K, Quiñones-Hinojosa A. The Cost of Brain Surgery: Awake vs Asleep Craniotomy for Perirolandic Region Tumors. Neurosurgery. 2017 Mar 15. doi: 10.1093/neuros/nyx022. [Epub ahead of print] PubMed PMID: 28327904.

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Motomura K, Natsume A, Iijima K, Kuramitsu S, Fujii M, Yamamoto T, Maesawa S, Sugiura J, Wakabayashi T. Surgical benefits of combined awake craniotomy and intraoperative magnetic resonance imaging for gliomas associated with eloquent areas. J Neurosurg. 2017 Jan 6:1-8. doi: 10.3171/2016.9.JNS16152. [Epub ahead of print] PubMed PMID: 28059650.

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Itoi C, Hiromitsu K, Saito S, Yamada R, Shinoura N, Midorikawa A. Predicting sleepiness during an awake craniotomy. Clin Neurol Neurosurg. 2015 Oct 31;139:307-310. doi: 10.1016/j.clineuro.2015.10.033. [Epub ahead of print] PubMed PMID: 26571456.

21)

Pereira LC, Oliveira KM, L’Abbate GL, Sugai R, Ferreira JA, da Motta LA. Outcome of fully awake craniotomy for lesions near the eloquent cortex: analysis of a prospective surgical series of 79 supratentorial primary brain tumors with long follow-up. Acta Neurochir (Wien). 2009 Oct;151(10):1215-30. doi: 10.1007/s00701-009-0363-9. PubMed PMID: 19730779.

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