|
| |
 |
|
| CASE REPORT |
|
| Year : 2020 | Volume
: 3
| Issue : 3 | Page : 143-148 |
|
Strategy of awake surgical resection for glioma based on intraoperative functional mapping and monitoring: A case report
Yingwu Shi, Shunnan Ge, Peigang Ji, Jinghui Liu, Yuan Wang, Shaochun Guo, Yulong Zhai, Min Chao, Guodong Gao, Yan Qu, Liang Wang
Department of Neurosurgery, Tangdu Hospital, Fourth Military Medical University, Xi'an, Shaanxi Province, China
| Date of Submission | 12-May-2020 |
| Date of Decision | 26-May-2020 |
| Date of Acceptance | 28-Jun-2020 |
| Date of Web Publication | 17-Oct-2020 |
Correspondence Address:
Dr. Liang Wang
Department of Neurosurgery, Tangdu Hospital, Fourth Military Medical University, No. 569, Xin Si Road, Xi'an 710038, Shaanxi Province
China
Shunnan Ge
Department of Neurosurgery, Tangdu Hospital, Fourth Military Medical University, No. 569 Xin Si Road, Xi'an 710038, Shaanxi Province
China
 Source of Support: None, Conflict of Interest: None
DOI: 10.4103/glioma.glioma_15_20
We reported a case of awake surgery for the left frontal low-grade glioma and reviewed the literature on the strategy of awake surgical resection for glioma. The eloquent cerebral areas that are involved in motor, language, memory, and visuospatial functions, which have to be preserved during surgery, is identified through intraoperative use of brain mapping techniques. This technique of combining intraoperative ultrasound and neuronavigation enabled extension of the surgical indications and improved the extent of resection, while minimizing postoperative morbidity and safeguarding the patient's quality of life. This work was approved by the Institutional Review Board of Tangdu Hospital, Fourth Military Medical University, China. Keywords: Awake surgery, brain mapping, intraoperative ultrasound, low-grade glioma, neuronavigation
How to cite this article:
Shi Y, Ge S, Ji P, Liu J, Wang Y, Guo S, Zhai Y, Chao M, Gao G, Qu Y, Wang L. Strategy of awake surgical resection for glioma based on intraoperative functional mapping and monitoring: A case report. Glioma 2020;3:143-8 |
How to cite this URL:
Shi Y, Ge S, Ji P, Liu J, Wang Y, Guo S, Zhai Y, Chao M, Gao G, Qu Y, Wang L. Strategy of awake surgical resection for glioma based on intraoperative functional mapping and monitoring: A case report. Glioma [serial online] 2020 [cited 2023 Apr 2];3:143-8. Available from: http://www.jglioma.com/text.asp?2020/3/3/143/298390 |
Yingwu Shi, Shunnan Ge, Peigang Ji are contributed equally.
| Introduction | |  |
Glioma is the most common primary brain tumor in adults and is often malignant. Awake craniotomy has been advocated for the resection of eloquent low-grade gliomas.[1] Moreover, the combination of neurophysiologic electrical mapping techniques during awake craniotomy has increased the number of cases of total and supratotal resection of low-grade gliomas, as well the overall survival rates.[2]
The eloquent brain areas that are related to memory, language, motor, and visuospatial functions, which have to be preserved in surgery, is identified through intraoperative use of brain mapping techniques.[3] Intraoperative neurophysiologic monitoring devices provide important detectable information for neurofunctional diagnosis. Such diagnostic imaging has been an important factor in decision-making under various situations.[4]
In this case report, we aimed to introduce the procedure and attentions of awake surgery for low-grade glioma in functional areas of the brain.
| Case Report | | |
Case
A 37-year-old woman was admitted because of one episode of seizure a month prior. She had no neurologic deficit preoperatively. She had no pertinent personal and family history.
Physical examination was unremarkable, and the language test was normal. Preoperative computed tomography (CT) and magnetic resonance imaging (MRI) showed a left frontal lobe tumor adjacent to the motor/language cortex [Figure 1]A, [Figure 1]B, [Figure 1]C. The magnetic resonance spectrum showed that the lesion had relatively high metabolic but low neuronal activities. The initial diagnosis was low-grade glioma. Before surgery, the patient received related education and training for better cooperation with her doctors. | Figure 1: Diagram of intraoperative ultrasound. During the operation, ultrasound is used to confirm the following: (A) the border of the tumor, (B) the border of the residual tumor, and (C) the extent of resection
Click here to view |
This study was conducted retrospectively, and approval for the study was obtained from the Institutional Review Board of Tangdu Hospital, Fourth Military Medical University, China. The patient singed informed consent.
Anesthetic management
Preoperatively, ropivacaine for anesthesia was administered to the superior orbital, auriculotemporal, deep temporal, greater occipital, and lesser occipital nerves. A Mayfield headstock was used to fix the brain, followed by infiltration of anesthetic on the scalp. The surgical incision was designed according to the neuronavigation. A pterional approach was applied, and local infiltration anesthesia was performed with ropivacaine. Intravenous propofol and remifentanil were administered preoperatively and throughout the surgery. According to the BISS results, anesthetic drug input was controlled in a targeted manner. A nasal catheter coated with lidocaine gel was routinely placed to facilitate airway management.
After skull removal, lidocaine cotton tablets were used to perform infiltration anesthesia on the surface of the dura mater for 2–3 min. After suspension of the dura, the intravenous anesthetic drugs were stopped; and 10–15 min later, the patient was fully awake.
Mapping and surgery
Before the dura incision after elevation of the bone flap, we again confirmed the tumor location by intraoperative ultrasound and neuronavigation to prepare the brain mapping. Before starting stimulation mapping, simultaneous electrophysiologic recordings of the cortical surface (i.e., electrocorticography) were placed around the eloquent areas to detect post-discharge caused by stimulation. Iced Ringer's solution was available on the surgical field for rapid termination of intraoperative seizures, as previously described.[5]
Cortical stimulation was delivered by a bipolar electrode, which began with 2 mA and was added to max until after-discharge potentials were detected on intraoperative mapping language or when motor or somatosensory function was established. 1.25 ms biphasic square waves in 4 s trains at 60 Hz were generated by a constant current generator. The stimulation was generated across 1 mm bipolar electrodes divided by 5 mm.
The stimulation of mapping began at an intensity of 2 mA and was added stepwise by 2 mA to a maximum of 10 mA, before claiming a specific cortical area to be passive for motor or language function. In active language mapping, the region was restimulated three times to reproduce the functional damage and to confirm the cortical region was necessary for language function. The higher limit to avoid intraoperative seizures was 10 mA, which was enough for positive eloquent language and motor cortex mapping. Besides, the stimulator directed at mapping had an upper limit of generating 10 mA.
After capturing the discharge potentials, the amplitude directed at stimulation was decreased by 2 mA, and the location that elicited the after-discharge potentials was avoided if no functional deficits were induced at that site. Locations that achieved mapping were not restimulated, and the adjacent cortical area was remapped for confirmation. For subcortical stimulation, we used the functional tract and arcuate fasciculus to confirm the distance from the tumor resection border to the functional tract intraoperatively. If the patient had a positive reaction with the stimulation at 4 mA, safe resection boundary was confirmed. In this way, we could safely extend the resection of nonfunctional peritumoral tissue.
Using the cortical stimulation methods mentioned above, we identified the respective motor and language cortex areas around the tumor, and the stimulation for the tumor lesion should be guaranteed as negative by ultrasound. In every positive site identified, tumor resection was performed up to 0.5 cm from the center of the stimulation site. In addition, subcortical stimulation was done to identify the pyramidal tract, and resection was stopped when stimulation with 6–8 mA was positive. Unless, it was necessary to access the tumor, the neurosurgeon did not resect the tissue that was not involved by the tumor.
Monitoring
Motor function was evaluated on the basis of the tumor location by requesting the patient to perform different movements, such as flexing the foot or clenching the fist, and according to the capacity of the patient to initiate and plan activities, in the event of deficits near to the supplementary motor cortex. Language testing such as counting was conducted to ensure the locations responsible for alexia, anomia, and speech arrest on stimulation. The definition of speech arrest is stopping in counting numbers without any simultaneous motor response (e.g., pharynx motor response). Continuing sites were stimulated for 3–4 s, with tasks divided by 4–10 s. Language monitoring was performed through various aspects of speech comprehension and production; these included counting numbers, repetition, and visual object recognition. The methods are described below.
Counting numbers was a simple language task, wherein patients were requested to count from 10 to 20, while mapping speech production. About 10–20 numerically marked simulation locations divided by 1 cm were positioned on the surgical field. Repetition and reading tasks used words and sentences. For the task of visual object recognition, patients were presented with and requested to name photographs of concrete objects, such as a banana or a car, from some semantic categories, such as clothing items or animals.
Intraoperative ultrasound to check for tumor resection
As shown in [Figure 1], intraoperative ultrasound was used before the dura incision to first confirm the tumor location and to design the dura incision. After resecting a part of the glioma, real-time ultrasound was used to check for residual glioma. After removal of residual glioma, we used ultrasound to judge the extent of resection.
| Results | | |
Pathologic findings
This patient underwent gross tumor resection with functional preservation, and she was kept asleep during closure. Compared to preoperative MRI [Figure 2]A and [Figure 2]B, postoperative MRI showed that the tumor had been totally removed [Figure 2]C and [Figure 2]D, and the pathologic diagnosis was oligodendroglioma (WHO II). The molecular pathology result showed IDH1 mut (+), 1q/19p co-del. | Figure 2: Preoperative and postoperative MRI of the patient (A–C) on preoperative MRI, there is a left frontal lobe tumor adjacent to the motor/language cortex (arrows). (D–F) Postoperative MRI shows the area of gross tumor resection (arrows). MRI: Magnetic resonance imaging
Click here to view |
Monitoring results
First, we ensured the motor border by cortical stimulation. [Figure 3] shows the responses after stimulation of the different areas of the cortex. In the motor cortex, stimulation caused twitching of the laryngeal muscle at point 1, tongue deviation at point 2, and mouth deflection and facial palsy at points 3 and 4. In the border of language cortex, stimulation caused language pause at points 5 and 7, calculation error at point 8, and difficulty in reading a picture at point 9. Subcortical stimulation was confirmed at points 11 and 12, which comprised the border of the pyramidal tract; when stimulation with 6 mA showed a positive motor response, the resection was stopped to preserve the motor function. | Figure 3: Determination of the tumor border and functional area by brain mapping. 1–4 represent the motor cortex, 5–9 represent the language cortex, and A–D represent the tumor border
Click here to view |
Postoperative MRI and recovery
Postoperative MRI [Figure 2]D, [Figure 2]E, [Figure 2]F showed complete tumor resection. The patient recovered well in a short time. There was good preservation of the motor and language functions, and the goal of maximal and safe tumor resection was achieved.
Postoperative management and follow-up
The patient underwent enhanced recovery after surgery,[6] which mainly included preoperative, intraoperative, and postoperative management. She recovered well and was able to walk independently 24 h postoperatively. Subsequently, the patient was observed and underwent regular MRI follow-up, according to the National Comprehensive Cancer Network Guidelines.
| Discussion | | |
Maximum range of safe resection is the principle of surgical resection of glioma. Studies have shown that resection of as many tumors as possible can effectively improve the survival time of patients with glioma.[7] The application of neuronavigation, intraoperative ultrasound guidance, fluorescence imaging, and intraoperative MRI can accurately locate the tumor and enable removal of as many tumors as possible.[8] For gliomas that are adjacent to a functional area, nerve function needs to be protected. Brain mapping is the golden standard to determine function of cortex. Cortical and subcortical stimulation techniques can identify the exact location of the functional cortex and subcortical conduction bundles to easily protect brain function.[9]
Intraoperative cortical stimulation may induce cortical discharge, which can result in epilepsy and in severe cases, acute encephalocele. Electrocorticography can be used for timely assessment of the neurophysiologic effects of stimulation of the complex and highly interconnected cerebral tissue during surgery. Washing the brain area with iced saline can alleviate a vast majority of epilepsy episodes. Moreover, avoiding continuous stimulation of the same brain region can reduce the occurrence of epilepsy.
Cortical mapping allows detecting the feasible mechanisms of brain reshaping that is generated by the tumor and the delineation of the individual limits of resection.[10] Continuous intraoperative neuropsychologic monitoring throughout the resection has been advocated, in order to check for any cognitive deficit and emerging neurologic online.[11] Besides, subcortical stimulation mapping in the patient can be used to preserve and detect the eloquent white matter pathways, and the deep gray matter nuclei.[2] Cortical mapping enables continued resection until the functional borders are reached at the cortical and subcortical levels, with no margin around the eloquent regions.[12] Compared to conventional surgery with no mapping, the strategy has been proved to optimize the benefit to risk ratio of surgery for gliomas by maximizing the extent of resection, both in noneloquent and eloquent areas, and by improving the median survival while minimizing the hazard for permanent deficits.[13] In this case, cortical and subcortical mapping was used to ensure the border of the tumor and enabled completed tumor resection with functional preservation. However, there were false-positive and false-negative results during cortical and subcortical stimulation.
The plastic potential is much more limited in the subcortical pathways than in the cortical areas, because white matter connectivity appears to be necessary for network redistribution.[14] Researches revealed that the functional influences of damage to the uncinate, middle longitudinal, and part of the inferior longitudinal fascicles can be compensated.[15],[16] In contrast, the structural integrity of the superior longitudinal, inferior fronto-occipital, and subcallosal fascicles need to be saved to prevent permanent functional neurologic damage.[17],[18] Hence, the functional role of these subcortical pathways need to be assessed using appropriate tasks. In this case, language cortex was ensured by naming and counting number. Because language in the cerebra is facilitated by a complex network, single language task, such as counting, is insufficient to strictly confirm the possible range of functions of a particular cerebra region in the language network.[19] Some researchers put forward the quick mixed test, which enables simultaneous screening of various language and nonlanguage functions, such as naming and movement in parallel, in a short period of time.[20],[21]
Because there may be a tradeoff between function preservation and the extent of resection, which is also called maximal safe tumor resection, the first suggestion is to discreetly make a tailored subcortical tasks, in view of tumor characteristics, such as anatomofunctional and location analysis, and the patient's characteristics, such as hobby and jobs.[22] Our present case was a professionally active patient, who want to recover normal professional activities after the surgery have individual onco-functional balance, compared to that in than older retired patients. Exploring the possible postoperative deficits in relation to the extent of resection between the neurosurgical doctors and the patients and their family are important.[23] The patient in this study had no special request; therefore, she underwent gross tumor resection with functional preservation.
Several researches have studied the accuracy and precision of functional MRI (fMRI), with high specificity and sensitivity in predicting function of motor cortex, compared with that of direct cortical stimulation.[24],[25] In some studies, motor fMRI has been demonstrated to be a reliable method to localize function of motor cortex, which can reduce the time needed for intraoperative mapping and facilitate surgical planning.[26] Anyway, there were also conflictive researches that showed a large deviation of fMRI-depicted areas, relative to the areas detected by electrophysiologic methods, such as direct cortical stimulation and navigated transcranial magnetic stimulation. These imply the need for critical thinking when using fMRI for preoperative planning. In addition, intraoperative ultrasound monitoring was used in this patient and enabled observation of the extent of resection.[27] In addition to CT and MRI, three-dimensional reconstruction was used to ensure the location of the tumor. Moreover, the information given by navigation determined the incision and increased the safety of surgery. Notably, loss of cerebrospinal fluid after dural incision can result in drifts and affect the application of neuronavigation. Intraoperative MRI can correct this condition, but it is expensive, inconvenient to operate, time consuming and laborious, and has not been popularized. A previous study showed that the fusion of three-dimensional ultrasound and neuronavigation for tumor localization can effectively reduce the navigation drift caused by cerebrospinal fluid loss and improve tumor localization.[28] During operation in this patient, ultrasound was used repeatedly to determine the border of the tumor. Compared with intraoperative nuclear MRI, ultrasound has several advantages, such as real-time imaging and lower cost.[29]
Currently, intraoperative electrical stimulation is the most reliable method of cortical mapping. Historically, areas with absent electrical activity should be removed to avoid postoperative complications. The limitation was later restricted to cerebra areas that are considered necessary for language functions, with the assumption that postoperative the deficits of language would not occur after resection of the cortical area that does not respond to stimulation.[30] That functional mapping was given on awake patients has allowed preservation or even improvement of the functional status, it has continued to improve importance, in the light of growing evidence on increased survival and quality of life. In this case, gross tumor resection was possible and short-term function was good. The effects of this strategy on long-term function need further study in the future.
Neurosurgeons usually could choose to debulk or resect an insular glioma, either by performing a craniotomy by awake craniotomy or under general anesthesia.[31] There had been no general consensus on the optimal protocol for anesthesia, but in terms of patient inconvenience during the surgical approach, an asleep-awake-asleep protocol might be superior.[32] In addition, general anesthesia has been preferred over awake craniotomy, because it has less challenges for the patients and has more advantages for the neurosurgeons. Moreover, general anesthesia is preferred for grade 4 gliomas, which are more often perivascular and have adhesions to the M2 and M3 branches of the middle cerebral artery. Because pressure on these branches is painful for patients who undergo awake craniotomy, general anesthesia has been typically used for grade 4 gliomas.[33] In other research, neurosurgeons found that awake craniotomy procedures were often quite long and led to patient fatigue, thereby, diminishing the advantages of awake surgery. Because craniotomy under general anesthesia has shown great results, doctors who have been satisfied with resecting these gliomas usually chose to use general anesthesia.[34] Nevertheless, awake craniotomy remains to be the preference for patients with frontal opercular extension, especially when the dominant frontal operculum is involved and in patients who developed speech problems after an epileptic insult.[35] In general, the dura mater is cut open when the patient is awake. In rare cases, epilepsy or acute encephalocele may occur when intravenous anesthesia is stopped.
Despite attempts to preserve preoperative skills and intraoperatively identify critical functions, the use of appropriate diagnostic methods was reported to result in high cognitive damage, which cannot be ignored.[36] Moreover, several recent studies have demonstrated frequent occurrence of memory and attention impairment, which have important roles in preserving good quality of life.[5] In awake surgery of glioma, good care is devoted to spare languages functions and to verify that the technique would achieve this objective. Less consideration has been devoted to preserving other cognitive functions, though impairment to praxis, working memory, attention, and executive skills, among others, will influence quality of life inevitably.[37] Besides, the evaluation of nonlinguistic cognitive abilities has received short emphasis in clinic, as demonstrated by the extensive use of the Karnofsky Performance Status Scale score for the assessment of quality of life, in spite of its known inadequacy, owing to its simplicity and design of measuring physical performance.[38] In another words, at present no defined standards for the evaluation of deficits in domains except language, although cognitive problems, compared with physical problems, have been convincingly shown to affect quality of life more. Some studies that used additional preoperative evaluation have demonstrated that rather than the effects of surgery, the effects of the tumor on cognition, especially verbal and visuospatial memory, attention, and executive functions, seemed to be more popular in the immediate postoperative phase.[39] These results suggested that detailed neuropsychologic testing is highly informative in patients with brain tumor.
Awake craniotomy for patients with glioma can be safely and effectively performed by combining intraoperative arousal, intraoperative ultrasound, and navigation. Accurate localization of tumor boundaries and functional areas to achieve the maximum range of total resection is critical for glioma surgery.
Institution review board statement
This work was approved by the Institutional Review Board of Tangdu Hospital, Fourth Military Medical University, China and conducted in concordance with the principles of the Declaration of Helsinki.
Declaration of patient consent
The authors certify that they have obtained the appropriate patient consent form. In the form, the patient has given her consent for her images and other clinical information to be reported in the journal. The patient understands that her name and initial will not be published and due efforts will be made to conceal his identity.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
| References | | |
| 1. | Wijnenga MM, French PJ, Dubbink HJ, Dinjens WN, Atmodimedjo PN, Kros JM, et al. The impact of surgery in molecularly defined low-grade glioma: An integrated clinical, radiological, and molecular analysis. Neuro Oncol 2018;20:103-12.  |
| 2. | Yordanova YN, Moritz-Gasser S, Duffau H. Awake surgery for WHO Grade II gliomas within “noneloquent” areas in the left dominant hemisphere: Toward a “supratotal” resection. Clinical article. J Neurosurg 2011;115:232-9. |
| 3. | Bertani G, Fava E, Casaceli G, Carrabba G, Casarotti A, Papagno C, et al. Intraoperative mapping and monitoring of brain functions for the resection of low-grade gliomas: Technical considerations. Neurosurg Focus 2009;27:E4. |
| 4. | Martino J, Gomez E, de Lucas EM, Mato D, Vázquez-Bourgon J. Intraoperative identification and preservation of verbal memory in diffuse gliomas: A matched-pair cohort study. Neurosurgery 2018;83:1209-18. |
| 5. | Minzenberg MJ, Poole JH, Vinogradov S, Shenaut GK, Ober BA. Slowed lexical access is uniquely associated with positive and disorganised symptoms in schizophrenia. Cogn Neuropsychiatry 2003;8:107-27. |
| 6. | Wang Y, Liu B, Zhao T, Zhao B, Yu D, Jiang X, et al. Safety and efficacy of a novel neurosurgical enhanced recovery after surgery protocol for elective craniotomy: A prospective randomized controlled trial. J Neurosurg 2018:1-2. |
| 7. | Hervey-Jumper SL, Berger MS. Maximizing safe resection of low- and high-grade glioma. J Neurooncol 2016;130:269-82. |
| 8. | Jenkinson MD, Barone DG, Bryant A, Vale L, Bulbeck H, Lawrie TA, et al. Intraoperative imaging technology to maximise extent of resection for glioma. Cochrane Database Syst Rev 2018;1:CD012788. |
| 9. | Moiyadi A, Velayutham P, Shetty P, Seidel K, Janu A, Madhugiri V, et al. Combined motor evoked potential monitoring and subcortical dynamic mapping in motor eloquent tumors allows safer and extended resections. World Neurosurg 2018;120:e259-68. |
| 10. | Rossini PM, Dal Forno G. Integrated technology for evaluation of brain function and neural plasticity. Phys Med Rehabil Clin N Am 2004;15:263-306. |
| 11. | Kristo G, Raemaekers M, Rutten GJ, de Gelder B, Ramsey NF. Inter-hemispheric language functional reorganization in low-grade glioma patients after tumour surgery. Cortex 2015;64:235-48. |
| 12. | Rivera-Rivera PA, Rios-Lago M, Sanchez-Casarrubios S, Salazar O, Yus M, González-Hidalgo M, et al. Cortical plasticity catalyzed by prehabilitation enables extensive resection of brain tumors in eloquent areas. J Neurosurg 2017;126:1323-33. |
| 13. | Gulati S, Jakola AS, Nerland US, Weber C, Solheim O. The risk of getting worse: Surgically acquired deficits, perioperative complications, and functional outcomes after primary resection of glioblastoma. World Neurosurg 2011;76:572-9. |
| 14. | Freyschlag CF, Duffau H. Awake brain mapping of cortex and subcortical pathways in brain tumor surgery. J Neurosurg Sci 2014;58:199-213. |
| 15. | Lemaitre AL, Lafargue G, Duffau H, Herbet G. Damage to the left uncinate fasciculus is associated with heightened schizotypal traits: A multimodal lesion-mapping study. Schizophr Res 2018;197:240-8. |
| 16. | Nakajima R, Kinoshita M, Miyashita K, Okita H, Genda R, Yahata T, et al. Damage of the right dorsal superior longitudinal fascicle by awake surgery for glioma causes persistent visuospatial dysfunction. Sci Rep 2017;7:17158. |
| 17. | Duffau H, Gatignol P, Moritz-Gasser S, Mandonnet E. Is the left uncinate fasciculus essential for language? A cerebral stimulation study. J Neurol 2009;256:382-9. |
| 18. | Chernoff BL, Teghipco A, Garcea FE, Sims MH, Paul DA, Tivarus ME, et al. A role for the frontal aslant tract in speech planning: A neurosurgical case study. J Cogn Neurosci 2018;30:752-69. |
| 19. | Duffau H. Contribution of cortical and subcortical electrostimulation in brain glioma surgery: Methodological and functional considerations. Neurophysiol Clin 2007;37:373-82. |
| 20. | Meier C, Lea SE, McLaren IP. Task-switching in pigeons: Associative learning or executive control? J Exp Psychol Anim Learn Cogn 2016;42:163-76. |
| 21. | 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) 2015;157:577-88. |
| 22. | Kelly PJ, Daumas-Duport C, Kispert DB, Kall BA, Scheithauer BW, Illig JJ. Imaging-based stereotaxic serial biopsies in untreated intracranial glial neoplasms. J Neurosurg 1987;66:865-74. |
| 23. | Law M, Oh S, Babb JS, Wang E, Inglese M, Zagzag D, et al. Low-grade gliomas: Dynamic susceptibility-weighted contrast-enhanced perfusion MR imaging--prediction of patient clinical response. Radiology 2006;238:658-67. |
| 24. | Fillard P, Descoteaux M, Goh A, Gouttard S, Jeurissen B, Malcolm J, et al. Quantitative evaluation of 10 tractography algorithms on a realistic diffusion MR phantom. Neuroimage 2011;56:220-34. |
| 25. | Yordanova YN, Cochereau J, Duffau H, Herbet G. Combining resting state functional MRI with intraoperative cortical stimulation to map the mentalizing network. Neuroimage 2019;186:628-36. |
| 26. | Heiervang E, Behrens TE, Mackay CE, Robson MD, Johansen-Berg H. Between session reproducibility and between subject variability of diffusion MR and tractography measures. Neuroimage 2006;33:867-77. |
| 27. | Ottenhausen M, Krieg SM, Meyer B, Ringel F. Functional preoperative and intraoperative mapping and monitoring: Increasing safety and efficacy in glioma surgery. Neurosurg Focus 2015;38:E3. |
| 28. | Chen F, Cui X, Liu J, Han B, Zhang D, Zhang X, et al. Tissue structure updating for In situ augmented reality navigation using calibrated ultrasound and two-level surface warping. IEEE Trans Biomed Eng 2020. doi: 10.1109/TBME.2020.2979535. |
| 29. | Duffau H. Lessons from brain mapping in surgery for low-grade glioma: Insights into associations between tumour and brain plasticity. Lancet Neurol 2005;4:476-86. |
| 30. | Santini B, Talacchi A, Squintani G, Casagrande F, Capasso R, Miceli G. Cognitive outcome after awake surgery for tumors in language areas. J Neurooncol 2012;108:319-26. |
| 31. | Gravesteijn BY, Keizer ME, Vincent AJPE, Schouten JW, Stolker RJ, Klimek M. Awake craniotomy versus craniotomy under general anesthesia for the surgical treatment of insular glioma: Choices and outcomes. Neurol Res 2018;40:87-96. |
| 32. | Joswig H, Bratelj D, Brunner T, Jacomet A, Hildebrandt G, Surbeck W. Awake craniotomy:First-year experiences and patient perception. World Neurosurg 2016;90:588-96. |
| 33. | Lu VM, Phan K, Rovin RA. Comparison of operative outcomes of eloquent glioma resection performed under awake versus general anesthesia: A systematic review and meta-analysis. Clin Neurol Neurosurg 2018;169:121-7. |
| 34. | Eseonu CI, Rincon-Torroella J, ReFaey K, Lee YM, Nangiana J, Vivas-Buitrago T, et al. Awake craniotomy vs craniotomy under general anesthesia for perirolandic gliomas: Evaluating perioperative complications and extent of resection. Neurosurgery 2017;81:481-9. |
| 35. | Arzoine J, Levé C, Pérez-Hick A, Goodden J, Almairac F, Aubrun S, et al. Anesthesia management for low-grade glioma awake surgery: A European Low-Grade Glioma Network survey. Acta Neurochir (Wien) 2020;162:1701-7. |
| 36. | Lewis RL, Vasishth S, Van Dyke JA. Computational principles of working memory in sentence comprehension. Trends Cogn Sci 2006;10:447-54. |
| 37. | Tensaouti F, Lahlou I, Clarisse P, Lotterie JA, Berry I. Quantitative and reproducibility study of four tractography algorithms used in clinical routine. J Magn Reson Imaging 2011;34:165-72. |
| 38. | Gabel N, Altshuler DB, Brezzell A, Briceño EM, Boileau NR, Miklja Z, et al. Health related quality of life in adult low and high-grade glioma patients using the National Institutes of Health Patient Reported Outcomes Measurement Information System (PROMIS) and Neuro-QOL Assessments. Front Neurol 2019;10:212. |
| 39. | Duffau H. Diffuse low-grade glioma, oncological outcome and quality of life: A surgical perspective. Curr Opin Oncol 2018;30:383-9. |
[Figure 1], [Figure 2], [Figure 3]
|
Related articles