|Year : 2022 | Volume
| Issue : 4 | Page : 113-119
Personal philosophy in glioma surgery and anatomo-functional mapping
George Samandouras1, Youkun Qian2, Viktoria Sefcikova3, Aisha Ghare4
1 UCL Queen Square Institute of Neurology, University College London; Victor Horsley Department of Neurosurgery, The National Hospital for Neurology and Neurosurgery, London, UK
2 Neurologic Surgery Department, Huashan Hospital, Shanghai Medical College, Fudan University; Shanghai Key Laboratory of Brain Function Restoration and Neural Regeneration; National Center for Neurological Disorders, Huashan Hospital, Shanghai Medical College, Fudan University, Shanghai, China
3 UCL Queen Square Institute of Neurology, University College London, UK; The University of Queensland Medical School, Brisbane, QLD, Australia
4 Victor Horsley Department of Neurosurgery, The National Hospital for Neurology and Neurosurgery, London, UK
|Date of Submission||27-Dec-2022|
|Date of Decision||16-Jan-2023|
|Date of Acceptance||17-Jan-2023|
|Date of Web Publication||08-Mar-2023|
Dr. George Samandouras
Victor Horsley Department of Neurosurgery, The National Hospital for Neurology and Neurosurgery, Queen Square, London
Source of Support: None, Conflict of Interest: None
|How to cite this article:|
Samandouras G, Qian Y, Sefcikova V, Ghare A. Personal philosophy in glioma surgery and anatomo-functional mapping. Glioma 2022;5:113-9
|How to cite this URL:|
Samandouras G, Qian Y, Sefcikova V, Ghare A. Personal philosophy in glioma surgery and anatomo-functional mapping. Glioma [serial online] 2022 [cited 2023 Apr 2];5:113-9. Available from: http://www.jglioma.com/text.asp?2022/5/4/113/371292
| Introduction|| |
Glioma surgery has evolved, during the last few decades, from diagnostic biopsies and limited debulking in noneloquent regions of the brain to maximum safe resections with advanced awake cognitive or asleep electrophysiological mapping.,,, This evolution has been supported by an increased understanding of molecular mechanisms of pathogenesis,,, the application of electrophysiological monitoring parameters,,, and engagement of the wider cognitive neuroscience community, as outputs of basic research and intraoperative electrical stimulation have been mutually beneficial in understanding cortical parcellation and network functionality.,,,,, No other neurosurgical specialty has undergone such a dramatic evolution in recent years. In this review, the experience and personal philosophy of the senior author will be described, along with practical points and technical nuances in navigating brain structure and function as applied to patients with supra- and infratentorial tumors.
| Awake Brain Mapping|| |
The value of awake brain mapping (ABM) in maximum safe resection of tumors affecting eloquent regions of the brain has been repeatedly documented in the literature and is currently considered a standard of care. However, despite a superficial veneer of uniformity, ABM is practiced with considerably different parameters across institutions, and even across practitioners in the same institution.
Our group recently published the results of a 20-question international survey on the domains of terminology as it pertains to the common understanding of clinical deficits, and the selection of intraoperative tests used per specific brain region. Examples among the twenty questions include deficits expected with stimulation of the dominant inferior frontal gyrus, corresponding to the historical area of Broca, or stimulation of the arcuate fasciculus. A low agreement was recorded for each of the twenty questions (Krippendorff's α = −0.023–0.312), regardless of specialism and years of practice, which reflects a wider uncertainty in the neuroscience community. Since the generation of Brodmann's cytoarchitectonic map, various subsequent brain parcellations with different variables, including functional neuroimaging, receptor, connectivity, and functional maps, have been proposed. However, a clinically validated brain map, either uni-or multi-parametric, remains elusive.,,, In other words, we have not yet succeeded in parcellating the cortex, assigning a function to each parcel, and nominating a reliable test to interrogate that particular parcel. This parallels the challenges in the subcortical white matter.
Our group recently published a review of the ventral language systems, incorporating data from direct electrical stimulation, diffusion magnetic resonance imaging (MRI), fiber dissection, autoradiography, neuropsychology, and cognitive neuroscience. During the year-long research of the literature, we encountered detailed datasets in sections of research, for example, diffusion MRI of white matter tracts, but the absence of integrative accounts and validation of white matter functional connectivity was evident. Therefore, surgeons performing direct electrical stimulation face an understandable uncertainty with specific testing paradigms. Caution is advised in occasionally reported oversimplification of function or mapping paradigms for common white matter tracts.
Similarly, a critical stance is required when outcomes of ABM are reported, as they may reflect considerably variable mapping paradigms with different tasks, error acceptance rates, and interpretation of outputs. Our group is in the process of completing an international multidisciplinary collaboration with cognitive neuroscience, functional neuroimaging, and high-volume surgery groups to propose a standardized brain map template with functional interrogation paradigms.
| Personalized Brain Mapping|| |
During the last few years, our group has introduced a novel, weekly multidisciplinary "awake brain mapping and complex tumor" meeting with the participation of neuropsychologists, cognitive neuroscientists, neurologists, speech and language therapists, functional neuroradiologists, MRI physicists, and neurosurgeons. Our models include input from neuropsychologists and speech and language therapists, based on preoperative assessments, voxel-based lesion-symptom mapping data, and previous datasets from our experience, resulting in a personalized mapping paradigm for each patient. Our intraoperative mapping results are banked into our existing database, correcting variability and smoothing an evolving probabilistic brain map.
| Illustrative Awake Brain Mapping Cases|| |
In all cases described and in accordance with the senior author's practice, our awake-throughout craniotomy technique reported previously, was employed. Patients receive a small amount of target-controlled infusion of propofol and remifentanil targeting blood concentrations of 0.8–1.2 mg/mL and 1–2 ng/mL, respectively, which is stopped following the application of the Mayfield clamp. Standard equipment used includes a microscope (Zeiss Kinevo 900, Zeiss, Oberkochen, Germany) and a 6-contact strip electrode (Ad-Tech Medical Instrument Corporation, Racine, USA) for electrocorticography and detection of after-discharge potentials. For motor and language mapping, mono-and bipolar stimulation were used, respectively (ISIS Xpert, inomed, Emmendingen, Germany).
Dominant supramarginal gyrus glioma
A 62-year-old male patient presented with dropping objects without being aware that his hand had opened; he had to look at his hand to maintain his grip. He had difficulty texting on his mobile and finally had a generalized tonic-clonic seizure. MRI scan showed an enhancing intrinsic tumor immediately underneath the supramarginal gyrus. Mapping paradigms were developed based on his personalized preoperative multidisciplinary assessment. These included, but were not limited to, motor, sensory functions and reaching and grasping testing, praxis with copying meaningless gestures, and working memory with reverse digit span. The four-parcel model of supramarginal gyrus parcellation based on voxel-based lesion-symptom mapping was used, including testing for repetition of pseudowords and nonwords, interrogating auditory short-term memory, and motor control of speech. During intraoperative testing, multiple eloquent areas were identified [Figure 1], allowing tumor resection through a narrow corridor inferior to the distal Sylvian vein, with no postoperative deficits. If a standard boston naming test had been used without personalized mapping paradigms, significant cognitive deficits would have occurred. The informed consent has been obtained from the patient.
|Figure 1: Preoperative MRI scans showing an enhancing tumor with a surface projection to the dominant supramarginal gyrus (A, top panel) and postoperative MRI sequences demonstrating T1 shortening with no additional enhancement (A, bottom panel). (B) Positive stimulation sites employing advanced cognitive mapping of praxis and reverse digit span allowed a narrow but safe surgical corridor. (C) Translation of the positive stimulation sites into our evolving brain map, with the segmentation of the supramarginal gyrus. AD: Anterior dorsal, AG: Angular gyrus, AV: Anterior ventral, PD: Posterior dorsal, PV: Posterior ventral, MRI: Magnetic resonance imaging, DLPF: Dorsolateral prefrontal cortex, PMv: Ventral premotor cortex. ©George Samandouras 2022|
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Dominant supplementary motor cortex, cingulum, corpus callosum glioma
Currently, there are no validated mapping paradigms for the cingulum or the corpus callosum, and the mapping paradigms for the supplementary motor area (SMA) and pre-SMA remain controversial., In the case described, a 38-year-old woman presented with cognitive and language difficulties. The tumor involved the dominant anterior cingulum and part of the genu and body of the corpus callosum. Following functional neuroimaging and assessment from the brain mapping MDT, personalized paradigms were proposed including SMA-based speech initiation using the sentence completion task. During surgery, the M1 was identified at 5 mA, while motor responses were obtained from the posterior SMA with slowness and twitching of the foot. Two discreet areas on SMA, marked with tickets #3 and #4, produced a consistent inability to complete sentences, while remarkably, stimulation of the same areas did not produce deficits on counting, articulation, or picture naming [Figure 2].
|Figure 2: MRI scan. (A) A nonenhancing lesion affecting the, SMA pre-SMA, cingulum, and corpus callosum with superimposed overlays of verb generation, verbal fluency, and the arcuate fasciculus. (B) Positive stimulation sites for speech initiation using the sentence completion test. (C) Anatomofuntional technique achieving complete ipsilateral resection of the affected cingulum and corpus callosum and skeletonization of the distal anterior cerebral arteries. (D) Postoperative MRI scan showing the extent of resection through a small cortical entry. Reprinted from Klitsinikos et al. with permission. MRI: Magnetic resonance imaging, SMA: Supplementary motor area|
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The functional variability of insular tumors
Surgical management of insular gliomas remains a challenge, attributed to the anatomy of the insula, enclosed by eloquent cortical parcels and encased by complex arterial and venous networks, its debated function, and the surrounding language and cognitive white matter tracts., Moreover, insular tumors approaches fall under two schools, either trans-Sylvian or trans-opercular. Our approach is based on two principles. First, a combined trans-Sylvian and trans-opercular approach gives the best results in our experience. With the Sylvian fissure split, the locations of all major arteries at risk are confirmed, allowing for their protection and radical tumor resection, while the cortical mapping allows for the creation of windows, usually one temporal and one frontal.
Our second principle is based on intraoperative anatomical and functional adaptability. In our cases, the cortical mapping reveals a dense cognitive function in frontal and temporal parcels allowing the creation of very small windows. Similarly, Sylvian fissure split has many variations based on the presence of cortical veins draining the inferior frontal gyrus, primarily temporal or frontal vein preference, and apposed or interdigitating gyri. Therefore, we are prepared in every case to adapt our approach to intraoperative findings by (1) creating large or very small cortical windows, (2) opening the Sylvian fissure widely or with gaps to protect cortical veins, and (3) moving the Sylvian vein toward the temporal or frontal sides. Finally, the identification and protection of the lateral lenticulostriate arteries (LLAs) require fine anatomical knowledge and tactile intelligence. The notion that LLAs should represent the medial edge of resection is, in our opinion, erroneous as tumors often, although not invariably, encase the LLAs and, therefore this will result in incomplete resections [Figure 3].
|Figure 3: Preoperative axial T2-weighted MRI scan. (A) A large dominant insular tumor. (B) Postoperative axial T2-weighted MRI shows resection. (C) Functional overlays demonstrate the tumor volume in purple and the arcuate fasciculus in orange with blue and green representing verb generation and verbal fluency regions. ©George Samandouras 2022. MRI: Magnetic resonance imaging|
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| Thalamocortical and Visual Mapping|| |
The current monitoring paradigms for sensory systems are based on basic, nonspecific monitoring of somatosensory evoked potentials in a way similar to all subspecialties, including spinal surgery. However, the disabling deficits of motor apraxia and sensory ataxia from intraoperative injury of the superior thalamocortical tracts result from a lack of specific techniques with region-specific, electrophysiological localization. My team and I have recently introduced a noninvasive technique for intraoperative localization and protection of the thalamocortical tracts. With this technique, we avoid the classical collision paradigm, in both asleep and awake craniotomies, and instead stimulate at the median, ulnar, or posterior tibial nerves while recordings are captured at the primary somatosensory cortex with a bipolar stimulation probe [Figure 4]. More data are required to further validate our technique.
|Figure 4: Electrophysiological monitoring of the right thalamocortical tract at the posterolateral margin of the resection cavity, successfully localizing and protecting the superior thalamocortical tract. M1: Primary motor cortex, S1: Primary somatosensory cortex. ©George Samandouras 2022|
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In mapping the optic radiations and visual cortex, we employ the classical visual evoked potential technique, but in addition, we employ the collision technique in asleep patients, producing positive localization of the optic radiation. An example of the collision technique using a navigated tubular retractor (NTR) for a lesion adjacent to the ependyma of the occipital horn of the lateral ventricle is demonstrated [Figure 5].
|Figure 5: Preoperative axial MRI scan. (A) A metastasis interfacing the optic radiation with a postoperative scan; (B) resection. (C) The tumor is nested between the parieto-occipital and calcarine sulci. (D) The tumor was removed with the use of a NTR (double arrow) to avoid retraction injury and the collision technique in addition to standard visual evoked potentials. The patient had no visual field defect postoperatively. ©George Samandouras 2022. MRI: Magnetic resonance imaging. NTR: navigated tubular retractor|
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| Vessel Preservation|| |
Successful brain mapping can be completely negated in the presence of a vascular event, from an arterial or venous stroke, even when small in size. Nationwide inpatient databases report that iatrogenic stroke and postoperative hematoma are among the most common complications in brain tumor surgery. Their incidence is 16.3/1000 and 10.3/1000, respectively. However, techniques for dissecting, preserving, and selectively obliterating arteries or veins traversing tumor volumes are rare in tumor surgery literature.
The senior author employs several techniques for arterial and venous skeletonization, even for small caliber vessels, including temporary clipping with awake or asleep neurophysiological monitoring to differentiate between en passant arteries or veins and tumoral vessels. There is a need to shift the operative philosophy to complete vessel preservation through meticulous dissections and test occlusion when necessary [Figure 6].
|Figure 6: Sagittal MRI scan. (A) A metastatic lesion (arrow) attached to the distal MCA. The MCA is skeletonized and isolated with vascular loops. (B) and is preserved (arrow) while the tumor is removed (C and D) Sagittal postoperative MRI scan shows tumor resection while the MCA (arrow) was preserved. ©George Samandouras 2022. MCA: Middle cerebral artery, MRI: Magnetic resonance imaging|
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| Deep-Seated Lesions and Navigated Tubular Retractor|| |
For small, deep-seated gliomas, our group employs NTR. Their main advantage is relatively atraumatic brain retraction compared to rigid retraction systems, as NTR increases the contact surface and distributes the pressure evenly along their circumference. NTR can optimize visibility, and their position can be dynamically adjusted. Rigid retraction systems have been associated with edema, ischemia, and even neurological deficits. In our practice, when we place the NTR in the eloquent cortex and white matter tracts, we advance the retractor millimeter by millimeter while performing direct electrical stimulation simultaneously. However, we found the indications are limited to small and deep-seated tumors [Figure 5]. In addition, NTR fixation is facilitated by the brain, and, in our opinion, more design modifications are required to increase the rigidity and improve NTR stabilization.
| En bloc Glioma Resection|| |
The senior author increasingly employs en-bloc resection of high-grade gliomas whenever possible. Some reports refer to perilesional resection with interestingly lower neurological deficits, even in eloquent brain regions. Our technique employs Rhoton microdissector #8 (Rhoton® Kit/Set) and suction to circumferentially develop and deepen the plane. When adjacent to a pial surface, the Velcro technique, described below, is used to empty the sulcal spaces and strip neural tissue from the pia. By preserving the tumor circumference, the volume of the tumor mobilizes and behaves as a single body, ultimately facilitating its en-bloc dissection.
| Fourth Ventricle, Brainstem, and Thalamic Tumors|| |
The increased attention in the awake and electrophysiological mapping of the supratentorial white matter tracts is not currently paralleled, at least to the same extent, to monitoring techniques of the cranial nerve (CN) nuclei and long tracts of the fourth ventricle and dorsal brainstem. This may be related to the attention of the wider neuroscience community to language and supratentorial white matter connectivity as opposed to brainstem nuclei and their connectivity. However, this remains paradoxical as neurological complications from intraoperative injury of these structures can result in unfavorable or, rarely, devastating outcomes. A report of an 18-year series of fourth ventricular tumors showed that 45% of patients had at least one major neurological deficit, including motor abnormalities or worsening gait (56%), speech or swallowing abnormalities (38%), or CN deficits (31%) such as CN VI-XII.
The practice of the senior author includes the resection of fourth ventricular ependymomas, medulloblastomas, brainstem and thalamic pilocytic astrocytomas, and pineal region tumors. Set up includes typical electrode placement with monitoring for CN III (inferior rectus, twisted pair subdermal 0.5 × 27 G), CN VII (orbicularis oculi and oris, with twisted pair subdermal 0.5 × 27 G), CN IX (in the soft palate bilaterally, with a double needle 2.5 mm), CN X (in endotracheal tube, TriVantage™, (Medtronic, Minneapolis, MN, USA), CN XI (upper trapezius with a twisted pair subdermal 0.5 × 27 G), and CN XII (tongue with a bipolar electrode 30 mm). In addition to routine free-running electromyography (EMG), we actively stimulate CN nuclei with triggered EMG, particularly in tumors infiltrating the floor of the fourth ventricle, allowing safe tumor resection. This technique is predicated on accurate anatomical knowledge of the predicted location of CN nuclei. Stimulation settings for triggered EMG that we employed include a sensitivity of 100 μV/div, and low frequency and high frequency of 50 and 1500 Hz, respectively. Our stimulation parameters are pulse duration of 200 μs and stimulation current of 0.2–2 mA, at 0.2 mA increments. In our experience, most responses are elicited at 1.5 mA.
In the posterior fossa, we prefer a telovelar approach by dividing the tela choroidea and inferior medullary velum.,, Most tumors widen the cerebello-medullary fissure facilitating the telovelar approach. We find trans-vermian approaches invasive and unnecessary. For thalamic tumors extending from the midbrain tegmentum, the senior author employs a tentorium-splitting supracerebellar/infratentorial approach in the sitting position with free running and triggered EMGs [Figure 7]. Our technique and anesthetic parameters for the sitting position have been previously reported.
|Figure 7: Preoperative sagittal MRI scan showing a large fourth ventricular/dorsal brainstem pilocytic astrocytoma (A) and postoperative appearances (B) following a supra-cerebellar infratentorial/transtentorial approach in the sitting position. ©George Samandouras 2022. MRI: Magnetic resonance imaging|
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| Tactile Intelligence|| |
One of the final points constituting a core in my personal philosophy is techniques on tissue handling. Practicing neurosurgeons have all skills in careful hand movements, safe handling of vessels, and protection of delicate structures. These skills run on a scale, and most can be learned. Some of the technical nuances I employ involve the use of suction as opposed to ultrasonic aspirators adjacent to expected arterial localization, for example, M1, M2, or LLAs with a standard aspiration setting of 20% or 20 kPa. This allows me to always have a standard reference on the cavitation effect on the normal versus gliotic tissue.
An indispensable instrument in my practice is the Rhoton micro-dissector #8. This allows me to manipulate and interrogate the neoplastic tissue, handle arteries, and empty sulci from their corresponding gyri. For example, the temporal gyri can be pulled down and away from the pia of the Sylvian fissure and middle cerebral artery with a combined action of the suction and Rhoton #8, in a movement I like to call the Velcro technique, ensuring a complete, atraumatic and pia-preserving technique. Finally, for more circumscribed tumors, I adhere to a plane, avoiding prodding the tumor with either the microdissector or the suction. This only causes unnecessary hemorrhage and distorts the plane. My principle is that if the surgeon respects the tumor by an atraumatic, perilesional dissection, then at the end, the tumor will facilitate its resection by revealing its borders, attachments, and complete extent.
| Conclusion|| |
My philosophy is centered on maximum tumor resection to minimize the risks of malignant transformation, for example in low-grade gliomas, while preserving the quality of life.,,,,, I employ anatomo-functional techniques based on detailed knowledge of anatomy, derived from my dissections and ongoing research and an effort to constantly integrate data outputs from cognitive neuroscience., These datasets are derived from constant interaction from clinical and research multidisciplinary groups I have built over the last several years., I find intraoperative neurophysiology reassuring when providing continuous, triggered feedback, particularly close to the corticospinal tract and CN nuclei. Delicate tissue handling and tactile intelligence facilitate tumor removal from adjacent, functionally and structurally, fragile structures. My research team maintains my enthusiasm to better understand critical research questions, while the trust and gratitude of my patients sustain and reward my efforts to fight with them in their challenging battles.
[Figure 1] and [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7] © George Samandouras 2022. No commercial use is permitted unless otherwise expressly granted.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Leon-Rojas JE, Ekert JO, Kirkman MA, Sewell D, Bisdas S, Samandouras G. Experience with awake throughout craniotomy in tumour surgery: Technique and outcomes of a prospective, consecutive case series with patient perception data. Acta Neurochir (Wien) 2020;162:3055-65.
Bickel S, Parvizi J. Electrical stimulation of the human claustrum. Epilepsy Behav 2019;97:296-303.
De Witt Hamer PC, Robles SG, Zwinderman AH, Duffau H, Berger MS. Impact of intraoperative stimulation brain mapping on Glioma surgery outcome: A meta-analysis. J Clin Oncol 2012;30:2559-65.
Simon MV, Nuwer MR, Szelényi A. Electroencephalography, electrocorticography, and cortical stimulation techniques. Handb Clin Neurol 2022;186:11-38.
Lasica AB, Jaunmuktane Z, Fersht N, Kirkman MA, Dixon L, Hoskote C, et al.
Genomic prognosticators and extent of resection in molecularly subtyped world health organization grade II and III gliomas-A single-institution, nine-year data. World Neurosurg 2021;151:e217-33.
Sefcikova V, Wong QH, Fersht N, Samandouras G. Commentary: Malignant pineal parenchymal tumors in adults: A national cancer database analysis. Neurosurgery 2022;91:e97-9.
Louis DN, Perry A, Wesseling P, Brat DJ, Cree IA, Figarella-Branger D, et al.
The 2021 WHO classification of tumors of the central nervous system: A summary. Neuro Oncol 2021;23:1231-51.
Viganò L, Callipo V, Lamperti M, Rossi M, Conti Nibali M, Sciortino T, et al.
Transcranial versus direct electrical stimulation for intraoperative motor-evoked potential monitoring: Prognostic value comparison in asleep brain tumor surgery. Front Oncol 2022;12:963669.
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.
Sefcikova V, Sporrer JK, Juvekar P, Golby A, Samandouras G. Converting sounds to meaning with ventral semantic language networks: Integration of interdisciplinary data on brain connectivity, direct electrical stimulation and clinical disconnection syndromes. Brain Struct Funct 2022;227:1545-64.
Samandouras G. Extended testing for cognition: Has awake brain mapping moved to the next level? Acta Neurochir (Wien) 2022;164:173-6.
Glasser MF, Rilling JK. DTI tractography of the human brain's language pathways. Cereb Cortex 2008;18:2471-82.
Catani M, Mesulam M. The arcuate fasciculus and the disconnection theme in language and aphasia: History and current state. Cortex 2008;44:953-61.
Dronkers NF. A new brain region for coordinating speech articulation. Nature 1996;384:159-61.
Heilman KM, Watson RT. The disconnection apraxias. Cortex 2008;44:975-82.
Sefcikova V, Sporrer JK, Ekert JO, Kirkman MA, Samandouras G. High interrater variability in intraoperative language testing and interpretation in awake brain mapping among neurosurgeons or neuropsychologists: An emerging need for standardization. World Neurosurg 2020;141:e651-60.
Zilles K, Amunts K. Centenary of Brodmann's map-conception and fate. Nat Rev Neurosci 2010;11:139-45.
Amunts K, Hawrylycz MJ, Van Essen DC, Van Horn JD, Harel N, Poline JB, et al.
Interoperable atlases of the human brain. Neuroimage 2014;99:525-32.
James GM, Gryglewski G, Vanicek T, Berroterán-Infante N, Philippe C, Kautzky A, et al.
Parcellation of the human cerebral cortex based on molecular targets in the serotonin system quantified by positron emission tomography in vivo
. Cereb Cortex 2019;29:372-82.
Desikan RS, Ségonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, et al.
An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 2006;31:968-80.
Uylings HB, Rajkowska G, Sanz-Arigita E, Amunts K, Zilles K. Consequences of large interindividual variability for human brain atlases: Converging macroscopical imaging and microscopical neuroanatomy. Anat Embryol (Berl) 2005;210:423-31.
Klitsinikos D, Ekert JO, Carels A, Samandouras G. Mapping and anatomo-surgical techniques for SMA-cingulum-corpus callosum gliomas; how I do it. Acta Neurochir (Wien) 2021;163:1239-46.
Nakajima R, Kinoshita M, Yahata T, Nakada M. Recovery time from supplementary motor area syndrome: Relationship to postoperative day 7 paralysis and damage of the cingulum. J Neurosurg 2019;132:865-74.
Spencer SS. Corpus callosum section and other disconnection procedures for medically intractable epilepsy. Epilepsia 1988;29 Suppl 2:S85-99.
Quinones-Hinojosa A, Chaichana KL, Mahato D. Brain Mapping: Indications and Techniques. New York: Thieme Medical Publishers, Incorporated; 2020.
Türe U, Yaşargil DC, Al-Mefty O, Yaşargil MG. Topographic anatomy of the insular region. J Neurosurg 1999;90:720-33.
Alexandratou A, Virjee RI, Ghare A, Sefcikova V, Micallef C, Mancini L, et al
. Intraoperative stimulation mapping of thalamocortical tracts in asleep and awake settings: Novel electrophysiological, anatomical and tractographic paradigms. J Neurosurg 2023. doi: 10.3171/2022.12.JNS221689.
De la Garza-Ramos R, Kerezoudis P, Tamargo RJ, Brem H, Huang J, Bydon M. Surgical complications following malignant brain tumor surgery: An analysis of 2002-2011 data. Clin Neurol Neurosurg 2016;140:6-10.
Al-Holou WN, Hodges TR, Everson RG, Freeman J, Zhou S, Suki D, et al.
Perilesional resection of glioblastoma is independently associated with improved outcomes. Neurosurgery 2020;86:112-21.
Shah A, Jhawar SS, Goel A. The lateral cerebral peduncle approach to ventrally placed intra-axial midbrain tumors: A technical note. J Clin Neurosci 2021;89:226-31.
Ferguson SD, Levine NB, Suki D, Tsung AJ, Lang FF, Sawaya R, et al.
The surgical treatment of tumors of the fourth ventricle: A single-institution experience. J Neurosurg 2018;128:339-51.
Sharma P, Sefcikova V, Sanders B, Soumpasis C, Waraich M, Samandouras G. Resection of ependymomas infiltrating the fourth ventricular floor: Anatomosurgical and stimulation mapping techniques. Oper Neurosurg (Hagerstown) 2022;22:e189-97.
Mussi AC, Matushita H, Andrade FG, Rhoton AL. Surgical approaches to IV ventricle-anatomical study. Childs Nerv Syst 2015;31:1807-14.
Mussi AC, Rhoton AL Jr. Telovelar approach to the fourth ventricle: Microsurgical anatomy. J Neurosurg 2000;92:812-23.
Pollack IF, Polinko P, Albright AL, Towbin R, Fitz C. Mutism and pseudobulbar symptoms after resection of posterior fossa tumors in children: Incidence and pathophysiology. Neurosurgery 1995;37:885-93.
Sharma P, Abdul M, Waraich M, Samandouras G. Pineal region tumours in the sitting position: How I do it. Acta Neurochir (Wien) 2022;164:79-85.
Loizidou M, Sefcikova V, Ekert JO, Bone M, Samandouras G. Reforming support systems of newly diagnosed brain cancer patients: A systematic review. J Neurooncol 2022;156:61-71.
Kim AA, Dono A, Khalafallah AM, Nettel-Rueda B, Samandouras G, Hadjipanayis CG, et al.
Early repeat resection for residual glioblastoma: Decision-making among an international cohort of neurosurgeons. J Neurosurg 2022;137:1618-27.
Ghaffari-Rafi A, Samandouras G. Effect of treatment modalities on progression-free survival and overall survival in molecularly subtyped World Health Organization grade II diffuse gliomas: A systematic review. World Neurosurg 2020;133:366-80.e2.
Sefcikova V, Christofi G, Samandouras G. Commentary: Postacute cognitive rehabilitation for adult brain tumor patients. Neurosurgery 2021;89:E295-7.
Taylor C, Ekert JO, Sefcikova V, Fersht N, Samandouras G. Discriminators of pseudoprogression and true progression in high-grade gliomas: A systematic review and meta-analysis. Sci Rep 2022;12:13258.
Vasilica AM, Sefcikova V, Samandouras G. Genetic alterations in non-syndromic, familial gliomas in first degree relatives: A systematic review. Clin Neurol Neurosurg 2020;198:106222.
Hasanov E, Yeboa DN, Tucker MD, Swanson TA, Beckham TH, Rini B, et al.
An interdisciplinary consensus on the management of brain metastases in patients with renal cell carcinoma. CA Cancer J Clin 2022;72:454-89.
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7]