|
| |
 |
|
| REVIEW |
|
| Year : 2022 | Volume
: 5
| Issue : 2 | Page : 62-68 |
|
Advanced modalities and surgical theories in glioma resection: A narrative review
Jiahe Guo1, Yiming Li1, Kai Zhang2, Jiabo Li3, Ping Liu1, Haolang Ming1, Yi Guo4, Shengping Yu1
1 Department of Neurosurgery, Tianjin Medical University General Hospital, Tianjin, China
2 Department of Surgery, First Teaching Hospital of Tianjin University of Traditional Chinese Medicine, Tianjin, China
3 Department of Pathology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA
4 Department of Neurosurgery, Tsinghua University Beijing Tsinghua Changgung Hospital, Beijing, China
| Date of Submission | 16-May-2022 |
| Date of Decision | 08-Jun-2022 |
| Date of Acceptance | 14-Jun-2022 |
| Date of Web Publication | 26-Jul-2022 |
Correspondence Address:
Prof. Shengping Yu
Department of Neurosurgery, Tianjin Medical University General Hospital, Tianjin
China
 Source of Support: None, Conflict of Interest: None
DOI: 10.4103/glioma.glioma_14_22
Surgical resection is the core of the comprehensive treatment of glioma. However, with infiltrative growth features, glioma often invades the surrounding area, making surgical resection more difficult. This review introduces relevant topics presented at the World Federation of Neurosurgical Societie Foundation Asian Congress of Neurological Surgeons (ACNS) Minimally Invasive Neurosurgery Web Seminar in 2022. First, we review assistive surgical techniques' characteristics, advantages, and disadvantages. Second, we summarize some state-of-the-art surgical views in glioma resection. Advanced modalities and surgical theories in glioma resection make better “maximum safe resection” achievable.
Keywords: Diffusion tensor imaging, fluorescence, functional mapping, functional magnetic resonance imaging, intraoperative diagnosis, lesion localization, magnetoencephalography, navigated transcranial magnetic stimulation, review, surgical theory
How to cite this article:
Guo J, Li Y, Zhang K, Li J, Liu P, Ming H, Guo Y, Yu S. Advanced modalities and surgical theories in glioma resection: A narrative review. Glioma 2022;5:62-8 |
How to cite this URL:
Guo J, Li Y, Zhang K, Li J, Liu P, Ming H, Guo Y, Yu S. Advanced modalities and surgical theories in glioma resection: A narrative review. Glioma [serial online] 2022 [cited 2023 Jun 9];5:62-8. Available from: http://www.jglioma.com/text.asp?2022/5/2/62/352255 |
| Introduction | |  |
Gliomas are the most frequent primary intracranial tumors. Surgical resection plays an essential role in the treatment process of glioma. Maximal safe resection can help improve the quality of life and prolong the overall survival (OS). The progression of surgical techniques, combined with the development of surgical theory, has brought glioma patients more safety and better prognosis. Advanced techniques are available at neurosurgeons' disposal today that achieves to maximize the extent of resection. Updated theories and recent publications have facilitated the decision-making in glioma resection. Therefore, we reviewed technologies widely used in glioma surgery (including preoperative and intraoperative techniques) and listed renewal surgical theories (preoperative planning, surgical removal, and boundary detection). We hope this review could provide beneficial information about perioperative technologies and surgical theories for neurosurgeons.
| Data Search Strategy | | |
The initial selection of literature was performed using PubMed database. Keywords search of this review including preoperative techniques, intraoperative techniques, surgical decision-making, surgical removal, and boundary of resection and other keywords were used to conduct a preliminary search of literature. Most of articles included in this review (85% of all references) were published from 2010 to 2022. The quality assessment of the literature was based on the author's clinical experience and knowledge. After initial selection and quality assessment, the review was conducted based on the included literature.
| Progressive Modalities in Glioma Resection | | |
Preoperative techniques
Diffusion tensor imaging
Protecting brain function in glioma surgery needs the preservation of white matter fibers and preoperative visualization of subcortical bundle fibers can facilitate the surgical planning and then protect them.[1] Diffusion tensor imaging (DTI) has been widely used in the preoperative reconstruction of white matter tracts.[2] In a randomized controlled trial of 238 high-grade glioma patients, fiber visualizing can improve the percentage of gross total resection (GTR), enhance the quality of life, and prolong the OS.[3] However, fiber tracking is limited by brain shift and perilesional edema,[4] while intraoperative correction (i.e., subcortical mapping) and advanced imaging techniques (i.e., diffusion spectrum imaging) can assist neurosurgeons to overcome those disadvantages.[5],[6] The application of DTI in glioma resection is shown in [Figure 1]. | Figure 1: Application of diffusion tensor imaging in glioma surgery. (A) Yellow: Tumor, Red: Inferior frontal gyrus and precentral gyrus, Blue: Vein; (B) Fibre tract marked by the curve in blue (corticospinal tract, corona radiata and cerebellothalamic tract), green (arcuate fasciculus), and pink (inferior logitudinal fasciculus and superior longitudinal fasciculus Ⅲ). Unpublished data
Click here to view |
Functional magnetic resonance imaging
Task-based blood-oxygen-level-dependent sequence, usually called functional magnetic resonance imaging MRI (fMRI), can localize function-specific cortices in our brain,[7] when performing tasks including picture naming, finger tapping, sentence comprehension, and verb generation. Functional MRI has a sensitivity of 37%–91% and specificity of 64%–83% for language mapping, as well as a sensitivity of 88%–100% and specificity of 66%–95% for motor mapping,[8],[9] while sometimes showing false-negative activations because of neurovascular uncoupling and potential neural plasticity.[10],[11] Although fMRI cannot determine the eloquent or rolandic area precisely, it provides helpful information for presurgical planning and predicative neuroplasticity.
Magnetoencephalography
Magnetoencephalography (MEG) is another technique to locate the functional cortex. Similar to the fMRI, MEG is also task-based. The magnetic fields caused by cortical activations could be visualized by MEG, which is valuable for surgical planning. Korvenoja et al. proved that MEG was better than fMRI, especially in identifying the central sulcus.[12] Nevertheless, MEG is less available with its higher cost in introducing the device and technical challenge in imaging interpretation.
Navigated transcranial magnetic stimulation
Navigated transcranial magnetic stimulation (nTMS) is a novel preoperative technique for functional localization, including a magnetic coil and a stereotactic image guidance navigation system. The appropriate current generated from the magnetic coil can lead to cortical excitement or inhibition. Research has proved that the motor cortex's accuracy detected by nTMS was 2.13 ± 0.29 mm.[13] In addition, Frey et al.[14] have reported that nTMS could increase the percentage of GTR from 42% to 59% and improve median progression-free survival from 15.4 to 22.4 months in the low-grade glioma group. However, nTMS needs experience and expertise in using the device and imaging interpretation. Navigated TMS for patients who suffered from glioma is shown in [Figure 2]. | Figure 2: Navigated transcranial magnetic stimulation for preoperative functional localization in patients with glioma. (A) Operation status in navigated transcranial magnetic stimulation, (B) location of the magnetic coil. Unpublished data
Click here to view |
The advantages and disadvantages of preoperative techniques are listed in [Table 1].
Intraoperative techniques
In addition to the preoperative techniques, numerous intraoperative techniques are worthy of investigation. Intraoperative techniques mainly include a navigating system, functional mapping, intraoperative diagnosis, and fluorescence.
Lesion localization
Neuronavigation
Neuronavigation can provide important information on tumor location and reveal cortical/subcortical invasion by integrating structural and functional images. In Wirtz CR's research, patients suffering from glioblastoma (GBM) achieved a higher GTR rate (31% vs. 19%) and lower residual cavity with neuronavigation.[15] On the other hand, neuronavigation has about 2–3 mm error on the final application accuracy, and surgeons are supposed to understand the power and limits and use them more properly.
Ultrasonography
The essential advantage of intraoperative ultrasound is its real-time performance. Except for boundary determination, ultrasonography can also assist neurosurgeons to verify the residual cavity after lesion resection.[16],[17],[18] Wang et al.[19] reported that high-grade glioma patients with intraoperative ultrasound use have higher 1-year and 2-year OS (59% and 33%) than those without ultrasound application (43% and 13%). The limitations of ultrasonography include a requirement of a specific facility, a longer learningcurve, and a lack of quantitative assessment. Intraoperative ultrasonography is illustrated in [Figure 3]. | Figure 3: Intraoperative ultrasonography for glioma surgery. (A) Boundary detection (lesion was marked by orange arrowheads). (B) Residual verification after lesion resection (residual cavity was marked by green arrowheads). Unpublished data
Click here to view |
Intraoperative Magnetic resonance imaging
Intraoperative MRI can provide high-resolution images for neurosurgeons. GTR was higher with intraoperative iMRI than those without.[20] A systematic review of GBM showed that iMRI could effectively improve the quality of life, extent of resection, and OS.[21] However, iMRI makes surgical time longer (+1 h) and has a higher cost.
Exoscope
Exoscope is a novel intraoperative technique. With a higher magnification rate, the advantage of exoscope in glioma surgery is evident.[22] With exoscope use, neurosurgeons can observe the same image on a specific display.[23] Despite the advantages of exoscope, the reliability of the microscope in deep lesion resection is still unique.
Functional mapping
Intraoperative stimulation mapping
Intraoperative stimulation mapping (ISM) is the gold standard for surgical localization in eloquent areas. With the use of ISM in glioma surgery, the percentage of GTR increased from 58% to 75%.[24] Except for ordinary general anesthesia, ISM can also use in awake surgery.[25] A high-quality meta-analysis showed that glioma surgery with ISM use was related to fewer late postoperative deficits and higher extent of resection.[24] However, we have to know that ISM still has some disadvantages. ISM needs a neuropsychologist to evaluate patients' conditions during the surgery. Furthermore, there are still some brain functions that cannot be assessed with ISM.
Somatosensory evoked potentials and motor evoked potentials
Electrophysiological monitoring, always includes somatosensory evoked potentials and motor evoked potentials, is widely used as a method of functional mapping. With higher permittivity and conductivity of glioma, electrophysiological monitoring can be used to assist in the determination of boundaries.[26] Intraoperative electrophysiological monitoring can decrease the postoperative neurological deficit and extend survival.[27]
Intraoperative diagnosis
Confocal laser endomicroscopy
Confocal laser endomicroscopy can assist neurosurgeons in diagnosing glioma with the unique feature of cellular and biological behavior.[28] In addition to intraoperative diagnosis, confocal laser endomicroscopy enables real-time interpretation of the boundary between normal and tumor at the resection cavity.[29]
Stimulated Raman histology
Stimulated Raman histology is a paramount intraoperative diagnostic technique for glioma. Stimulated Raman histology increased the Raman scattering signal through its nonlinear optical process, and has better monitoring speed and sensitivity.[30],[31]
Fluorescence
5-Aminolevulinic acid: Illuminating probes lead to the advent of fluorescence-guided surgery. One of the most widely used medications is 5-aminolevulinic acid (5-ALA).[16],[32] In the surgical process, extraneous 5-ALA can cause the accumulation of phototoxic protoporphyrin IX. The red fluorescence emitted by phototoxic protoporphyrin IX in glioma is conductive to the determination. With fluorescence with 5-ALA, neurosurgeons could easier differentiate the boundary between tumor and normal brain tissue. A phase III clinical trial proved that fluorescence-guided surgery with 5-ALA used has achieved a higher percentage of GTR than those with white-light microsurgery (65% vs. 36%).[32] Even though 5-ALA is beneficial to glioblastoma surgery, its sensitivity in low-grade glioma surgery is lower.
Fluorescein sodium
Another significant fluorescence is fluorescein sodium (FS). The damage to the blood–brain barrier, which often occurs in high-grade glioma, causes the leakage of FS. Hence, FS always accumulates and surrounds the lesion area.[33] A prospective phase Ⅱ clinical trial showed that FS-guided surgery is related to a higher percentage of GTR.[34] Compared with 5-ALA, FS is worse for its lower sensitivity and specificity.
The advantages and disadvantages of intraoperative techniques are listed in [Table 2].
| Advanced Surgical Theory in Glioma Resection | | |
Surgical decision making: Resection or biopsy
Published clinical guidelines from different national or international neurosurgical societies had standardized clinical glioma management.[35],[36],[37],[38] Surgical strategy for glioma still varies among institutions, which requires balancing individual patient characteristics and the surgeon's personal experience to determine the optimal treatment. Hence, many options are available, including supra-total resection, gross-total resection, partial resection, biopsy, and palliative care without surgery. Histopathological diagnosis is the mainstay of glioma treatment, and consequently, surgical resection or biopsy is preferred. Multicenter research summarized lesion location characteristics and the real-world clinical practice by Müller et al.[39] Biopsy decisions reached an agreement for tumors infiltrating the middle and posterior corpus callosum with contralateral tumor extension, the thalamus, and left the peri-atrial region. Resection decisions were made when tumors involved prefrontal, temporal, and right parietal cortices but not the medial precentral gyrus, the corona radiata of the corticospinal tract, and the left superior temporal gyrus. A study analyzed the propensity of 224 neurosurgeons in surgical decision-making for GBM patients by investigating multiple factors from the surgeon's view.[40] The patient's age is a factor worthy of attention in surgical decision-making because of the different goals in younger and older GBM patients, and the multidisciplinary neuro-oncology tumor board is duty-bound to develop a comprehensive treatment proposal.[17] A new staging system for neuroepithelial tumors by anatomical phenotyping may contribute to future neurosurgical decisions.[41]
Surgical removal: Peri- versus intralesional approach
In surgical oncology, perilesional or “en bloc” resection is a general principle aiming to remove a tumoral mass along with the continuous layer of healthy tissue. In brain tumors, dissection in the gliotic interface ensures GTR of brain metastasis due to the lack of infiltration. Such an approach to gliomas has not been widely proposed. The Intralesional or “piecemeal” debulking technique is preferred for glioma involving the eloquent areas, which is safer.[42] However, circumferential perilesional resection proved a valuable technique associated with higher rates of GTR of GBM and a lower rate of neurological complications than intralesional procedure, even in the eloquent areas.[43],[44] Notably, perilesional resection was significantly correlated with a lower intraoperative blood loss, which might be more appropriate for patients with poor surgical tolerance, like the elderly or children.
When performing “en bloc” resection in glioma, intraoperative ultrasound and the neuro-navigation system can help neurosurgeons identify the tumor's cortical margins and its subcortical extension,[45] followed by direct cortical mapping for further functional localization.[24] Along the edge of gyri, a subpial dissection technique allows the preservation of the vessels at the cortical and subcortical level by coagulating feeding vessels and avoiding vessels en passage.[43],[44] Operators identify the white matter interface from the perilesional tissue according to the color, texture, and bleeding until the white matter is encountered at the deep surface. The perilesional technique of glioma resection is shown in [Figure 4]. Protection of large or essential draining veins depends on hollow-carved resection work [Figure 5]. | Figure 4: “En Bloc” Resection of glioma. (A) Microscopic view of an LGG. (B) Subpial dissection. (C) Perilesional resection from sulcus to sulcus. (D) Bottom dissection. Unpublished data. LGG: Low-grade glioma
Click here to view |
 | Figure 5: “Hollow-craved” resection of glioma. (A) Subvenous dissection. (B) Isolated draining vein. Unpublished data
Click here to view |
Boundary of resection: Forward step to maximal safe resection
Surgical resection of glioma aims to maximize the extent of tumor resection while minimizing the risk of postoperative neurological sequelae. Surgeons have to find a delicate balance between these two conflicting goals. Nevertheless, we could do better with the updating radiological technology and insight into the functional neural plasticity.
Achieving maximum: Radiological guidance to the molecular boundary
The extent of resection stays a paramount prognostic factor for long-term outcomes, not only for glioblastoma[46],[47],[48] but also for low-grade glioma.[49] Radiologically, T1-weighted contrast-enhanced imaging for high-grade glioma and the T2 fluid-attenuated inversion recovery sequence for low-grade glioma are frequently utilized in glioma visualization and assisted tumor resection. However, conventional MRI sequences cannot outline the actual pathological boundary of glioma, limiting the surgical treatment of glioma. Autopsy reports show that 75% of patients have infiltrated GBM tumor cells in the contralateral hemisphere.[50] Tumor cells of low-grade glioma infiltrated along the white matter tracts and even extended to the radiological border delineated by the T2 fluid-attenuated inversion recovery imaging.[51] For glioma adjacent to the eloquent area, tailored resection along the onco-functional interface under awake craniotomy remains the gold standard of glioma resection, achieving maximal safe resection. However, when it comes to the glioma involving the non-eloquent area, supratotal resection, an aggressive resection beyond the margin defined by T1-weighted contrast-enhanced or FLAIR abnormalities, can further improve the OS.[46],[47],[48],[49] There is still no well-accepted cut-off edge of supratotal glioma resection at present. Here are some definitions: First, FLAIR-ectomy, resection amounting to all enhanced and FLAIR abnormalities;[52] second, resection until the encountered cortico-subcortical eloquent structures;[49] anatomic lobectomy in the noneloquent areas.[48] According to the fifth edition of the WHO Classification of Tumors of the Central Nervous System (WHO CNS5),[53] mutant isocitrate dehydrogenase (IDH-mut) becomes a necessary molecular marker for diagnosing adult diffuse low-grade glioma. Hypothetically, IDH-mut positive stained areas are supposed to be the actual tumor boundary. A novel imaging biomarker, called blood-oxygen-level-dependent asynchrony, can quantify a robust correlation between vascular dysregulation in resting-state blood-oxygen-level-dependent fMRI dynamics and IDH-mutant positive areas, which predicted a more significant margin identified on standard-of-care MRI.[54] Such research suggested that FLAIR hyperintensity may not be optimal for guiding treatment in this subset of gliomas. Furthermore, survival benefit from supratotal resection under the molecular boundary guidance needs further confirmation.
Neural integrity preservation: Functional mapping to brain plasticity
Glioma is generally considered an infiltrating disease instead of a well-defined tumor mass. Tumor cells extend beyond image-defined boundaries in low-grade glioma, throughout the hemisphere, and even contralaterally in glioblastoma. Ongoing glioma surgery is struggling for the optimal balance between tumor removal and neurologic compromise. We used to mistake that any damage to highly specialize functional areas, called “eloquent” regions, certainly causes major permanent neurological deficits, such as aphasia or hemiplegia. However, patients are likely to avoid postoperative functional deficits under glioma resection that involves “eloquent” cortex, such as Broca's area,[55] Wernicke's area,[56] and even Rolandic area.[57] The brain, a comprehensive network, involves dynamically producing, remodeling, and eliminating information.
When neurosurgeons remove the diffuse glioma, they have to concern with brain functions in the physiological and pathophysiological conditions. Glioma-related neuroplasticity is thought to exist during the whole pathophysiological process. Only a better understanding of the potential of neural plasticity can lead to more aggressive tumor removal:
(1) We must recognize that the neural plasticity potential is hierarchical, i.e., the cortex greater than the subcortical fiber, the cognitive cortex greater than the basic functional cortex, and projective fibers greater than bundle fibers.
(2) Neural remodeling is characterized by recruitment, from near to far, i.e., (1) intrinsic reorganization within glioma, (2) redistribution around the tumor, (3) remote compensation within the injured hemisphere, and (4) remote remodeling in the contralateral hemisphere.[58]
(3) Functional and structural redundancy launches the important material basis for neural plasticity.[59]
The cost to obtain satisfactory functional results is sometimes to perform incomplete resection when the glioma invades “unresectable” areas. However, functional plasticity enables an increased extent of resection in eloquent structures so far considered “inoperable.” Recently, Picart and coworkers envisaged a dynamic resection strategy for brain tumors, and their study demonstrated its potential in clinical practice.[60] Although the tailored multistage approaches for gliomas in the eloquent area are reliable, iterative resection is more painful for patients and faces more complex perioperative management than the one-stage approach. For lacking reliable prediction on the potential of neuroplasticity, neurosurgeons are “cautious” when removing the tumor in eloquent areas at the technical level and more willing to show functional integrity during awake surgery and immediately after operation. Multistage resection is not the final stage of diffuse glioma surgery. In the future, reliable prediction on the potential of neuroplasticity can further help us to resect more tumor tissue without continuous neurological sequelae.
| Limitations | | |
This review summarized previous researches on advanced modalities and surgical theories in glioma resection. Incomplete retrieval of identified research may exist in the narrative review due to the reporting bias and author bias, which can cause the omission of literature research.
| Conclusion | | |
Multi-modality techniques had been the “basic options” in glioma surgery, which allowed neurosurgeons to remove glioma more safely and efficiently. Surgeons should change their minds and focus more on normal brain tissue than the tumor itself so that a greater extent of glioma resection can finally be achieved.
Acknowledgments
Nil.
Financial support and sponsorship
The work was funded by the National Key Research and Development Program of China (No. 2018YFC0115603) and Clinical Medicine Research Project of Tianjin Medical University of China (No. 2018kylc001).
Conflicts of interest
There are no conflicts of interest.
| References | | |
| 1. | Buchmann N, Gempt J, Stoffel M, Foerschler A, Meyer B, Ringel F. Utility of diffusion tensor-imaged (DTI) motor fiber tracking for the resection of intracranial tumors near the corticospinal tract. Acta Neurochir (Wien) 2011;153:68-74.  |
| 2. | Li Y, Zhang W. Quantitative evaluation of diffusion tensor imaging for clinical management of glioma. Neurosurg Rev 2020;43:881-91. |
| 3. | Wu JS, Zhou LF, Tang WJ, Mao Y, Hu J, Song YY, et al. Clinical evaluation and follow-up outcome of diffusion tensor imaging-based functional neuronavigation: A prospective, controlled study in patients with gliomas involving pyramidal tracts. Neurosurgery 2007;61:935-48. |
| 4. | Romano A, D'Andrea G, Calabria LF, Coppola V, Espagnet CR, Pierallini A, et al. Pre-and intraoperative tractographic evaluation of corticospinal tract shift. Neurosurgery 2011;69:696-704. |
| 5. | Wedeen VJ, Hagmann P, Tseng WY, Reese TG, Weisskoff RM. Mapping complex tissue architecture with diffusion spectrum magnetic resonance imaging. Magn Reson Med 2005;54:1377-86. |
| 6. | Maesawa S, Fujii M, Nakahara N, Watanabe T, Wakabayashi T, Yoshida J. Intraoperative tractography and motor evoked potential (MEP) monitoring in surgery for gliomas around the corticospinal tract. World Neurosurg 2010;74:153-61. |
| 7. | Logothetis NK. What we can do and what we cannot do with fMRI. Nature 2008;453:869-78. |
| 8. | Kuchcinski G, Mellerio C, Pallud J, Dezamis E, Turc G, Rigaux-Viodé O, et al. Three-tesla functional MR language mapping: Comparison with direct cortical stimulation in gliomas. Neurology 2015;84:560-8. |
| 9. | Trinh VT, Fahim DK, Maldaun MV, Shah K, McCutcheon IE, Rao G, et al. Impact of preoperative functional magnetic resonance imaging during awake craniotomy procedures for intraoperative guidance and complication avoidance. Stereotact Funct Neurosurg 2014;92:315-22. |
| 10. | Ulmer JL, Hacein-Bey L, Mathews VP, Mueller WM, DeYoe EA, Prost RW, et al. Lesion-induced pseudo-dominance at functional magnetic resonance imaging: Implications for preoperative assessments. Neurosurgery 2004;55:569-79. |
| 11. | Azad TD, Duffau H. Limitations of functional neuroimaging for patient selection and surgical planning in glioma surgery. Neurosurg Focus 2020;48:E12. |
| 12. | Korvenoja A, Kirveskari E, Aronen HJ, Avikainen S, Brander A, Huttunen J, et al. Sensorimotor cortex localization: Comparison of magnetoencephalography, functional MR imaging, and intraoperative cortical mapping. Radiology 2006;241:213-22. |
| 13. | Tarapore PE, Tate MC, Findlay AM, Honma SM, Mizuiri D, Berger MS, et al. Preoperative multimodal motor mapping: A comparison of magnetoencephalography imaging, navigated transcranial magnetic stimulation, and direct cortical stimulation. J Neurosurg 2012;117:354-62. |
| 14. | Frey D, Schilt S, Strack V, Zdunczyk A, Rösler J, Niraula B, et al. Navigated transcranial magnetic stimulation improves the treatment outcome in patients with brain tumors in motor eloquent locations. Neuro Oncol 2014;16:1365-72. |
| 15. | Wirtz CR, Albert FK, Schwaderer M, Heuer C, Staubert A, Tronnier VM, et al. The benefit of neuronavigation for neurosurgery analyzed by its impact on glioblastoma surgery. Neurol Res 2000;22:354-60. |
| 16. | Hervey-Jumper SL, Berger MS. Maximizing safe resection of low-and high-grade glioma. J Neurooncol 2016;130:269-82. |
| 17. | Sastry R, Bi WL, Pieper S, Frisken S, Kapur T, Wells W 3 rd, et al. Applications of ultrasound in the resection of brain tumors. J Neuroimaging 2017;27:5-15. |
| 18. | Giammalva GR, Ferini G, Musso S, Salvaggio G, Pino MA, Gerardi RM, et al. Intraoperative ultrasound: Emerging technology and novel applications in brain tumor surgery. Front Oncol 2022;12:818446. |
| 19. | Wang J, Liu X, Ba YM, Yang YL, Gao GD, Wang L, et al. Effect of sonographically guided cerebral glioma surgery on survival time. J Ultrasound Med 2012;31:757-62. |
| 20. | Wu JS, Gong X, Song YY, Zhuang DX, Yao CJ, Qiu TM, et al. 3.0-T intraoperative magnetic resonance imaging-guided resection in cerebral glioma surgery: Interim analysis of a prospective, randomized, triple-blind, parallel-controlled trial. Neurosurgery 2014;61 Suppl 1:145-54. |
| 21. | Kubben PL, ter Meulen KJ, Schijns OE, ter Laak-Poort MP, van Overbeeke JJ, van Santbrink H. Intraoperative MRI-guided resection of glioblastoma multiforme: A systematic review. Lancet Oncol 2011;12:1062-70. |
| 22. | Langer DJ, White TG, Schulder M, Boockvar JA, Labib M, Lawton MT. Advances in intraoperative optics: A brief review of current exoscope platforms. Oper Neurosurg (Hagerstown) 2020;19:84-93. |
| 23. | Montemurro N, Scerrati A, Ricciardi L, Trevisi G. The exoscope in neurosurgery: An overview of the current literature of intraoperative use in brain and spine surgery. J Clin Med 2021;11:223. |
| 24. | 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. |
| 25. | Sacko O, Lauwers-Cances V, Brauge D, Sesay M, Brenner A, Roux FE. Awake craniotomy versus surgery under general anesthesia for resection of supratentorial lesions. Neurosurgery 2011;68:1192-8. |
| 26. | Pan SY, Chen JP, Cheng WY, Lee HT, Shen CC. The role of tailored intraoperative neurophysiological monitoring in glioma surgery: A single institute experience. J Neurooncol 2020;146:459-67. |
| 27. | Zhang ZZ, Shields LB, Sun DA, Zhang YP, Hunt MA, Shields CB. The art of intraoperative glioma identification. Front Oncol 2015;5:175. |
| 28. | Mooney MA, Zehri AH, Georges JF, Nakaji P. Laser scanning confocal endomicroscopy in the neurosurgical operating room: A review and discussion of future applications. Neurosurg Focus 2014;36:E9. |
| 29. | Breuskin D, Szczygielski J, Urbschat S, Kim YJ, Oertel J. Confocal laser endomicroscopy in neurosurgery – An alternative to instantaneous sections? World Neurosurg 2017;100:180-5. |
| 30. | Hollon TC, Pandian B, Urias E, Save AV, Adapa AR, Srinivasan S, et al. Rapid, label-free detection of diffuse glioma recurrence using intraoperative stimulated Raman histology and deep neural networks. Neuro Oncol 2021;23:144-55. |
| 31. | Di L, Eichberg DG, Huang K, Shah AH, Jamshidi AM, Luther EM, et al. Stimulated Raman histology for rapid intraoperative diagnosis of gliomas. World Neurosurg 2021;150:e135-43. |
| 32. | Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F, Reulen HJ, et al. Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: A randomised controlled multicentre phase III trial. Lancet Oncol 2006;7:392-401. |
| 33. | Stummer W, Novotny A, Stepp H, Goetz C, Bise K, Reulen HJ. Fluorescence-guided resection of glioblastoma multiforme by using 5-aminolevulinic acid-induced porphyrins: A prospective study in 52 consecutive patients. J Neurosurg 2000;93:1003-13. |
| 34. | Acerbi F, Broggi M, Eoli M, Anghileri E, Cuppini L, Pollo B, et al. Fluorescein-guided surgery for grade IV gliomas with a dedicated filter on the surgical microscope: Preliminary results in 12 cases. Acta Neurochir (Wien) 2013;155:1277-86. |
| 35. | Jiang T, Nam DH, Ram Z, Poon WS, Wang J, Boldbaatar D, et al. Clinical practice guidelines for the management of adult diffuse gliomas. Cancer Lett 2021;499:60-72. |
| 36. | Mohile NA, Messersmith H, Gatson NT, Hottinger AF, Lassman A, Morton J, et al. Therapy for diffuse astrocytic and oligodendroglial tumors in adults: ASCO-SNO guideline. J Clin Oncol 2022;40:403-26. |
| 37. | Nabors LB, Portnow J, Ahluwalia M, Baehring J, Brem H, Brem S, et al. Central nervous system cancers, version 3.2020, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw 2020;18:1537-70. |
| 38. | Weller M, van den Bent M, Preusser M, Le Rhun E, Tonn JC, Minniti G, et al. EANO guidelines on the diagnosis and treatment of diffuse gliomas of adulthood. Nat Rev Clin Oncol 2021;18:170-86. |
| 39. | Müller DM, Robe PA, Ardon H, Barkhof F, Bello L, Berger MS, et al. On the cutting edge of glioblastoma surgery: Where neurosurgeons agree and disagree on surgical decisions. J Neurosurg 2022;136:45-55. |
| 40. | Gerritsen JK, Broekman ML, De Vleeschouwer S, Schucht P, Jungk C, Krieg SM, et al. Decision making and surgical modality selection in glioblastoma patients: An international multicenter survey. J Neurooncol 2022;156:465-82. |
| 41. | Akeret K, Vasella F, Staartjes VE, Velz J, Müller T, Neidert MC, et al. Anatomical phenotyping and staging of brain tumours. Brain 2022;145:1162-76. |
| 42. | You H, Qiao H. Intraoperative neuromonitoring during resection of gliomas involving eloquent areas. Front Neurol 2021;12:658680. |
| 43. | 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. |
| 44. | Mishra A, Janu A, Trivedi K, Shetty P, Singh V, Moiyadi A. Subpial en bloc resection improves extent of resection in infiltrating gliomas – A propensity matched comparative cohort analysis. Clin Neurol Neurosurg 2022;215:107197. |
| 45. | Dixon L, Lim A, Grech-Sollars M, Nandi D, Camp S. Intraoperative ultrasound in brain tumor surgery: A review and implementation guide. Neurosurg Rev 2022; doi: 10.1007/s10143-022-01778-4. |
| 46. | Li YM, Suki D, Hess K, Sawaya R. The influence of maximum safe resection of glioblastoma on survival in 1229 patients: Can we do better than gross-total resection? J Neurosurg 2016;124:977-88. |
| 47. | Jackson C, Choi J, Khalafallah AM, Price C, Bettegowda C, Lim M, et al. A systematic review and meta-analysis of supratotal versus gross total resection for glioblastoma. J Neurooncol 2020;148:419-31. |
| 48. | Shah AH, Mahavadi A, Di L, Sanjurjo A, Eichberg DG, Borowy V, et al. Survival benefit of lobectomy for glioblastoma: Moving towards radical supramaximal resection. J Neurooncol 2020;148:501-8. |
| 49. | 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. |
| 50. | Claes A, Idema AJ, Wesseling P. Diffuse glioma growth: A guerilla war. Acta Neuropathol 2007;114:443-58. |
| 51. | Zetterling M, Roodakker KR, Berntsson SG, Edqvist PH, Latini F, Landtblom AM, et al. Extension of diffuse low-grade gliomas beyond radiological borders as shown by the coregistration of histopathological and magnetic resonance imaging data. J Neurosurg 2016;125:1155-66. |
| 52. | Pessina F, Navarria P, Cozzi L, Ascolese AM, Simonelli M, Santoro A, et al. Maximize surgical resection beyond contrast-enhancing boundaries in newly diagnosed glioblastoma multiforme: Is it useful and safe? A single institution retrospective experience. J Neurooncol 2017;135:129-39. |
| 53. | 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. |
| 54. | Petridis PD, Horenstein CI, Pereira B, Wu PB, Samanamud J, Marie T, et al. BOLD asynchrony elucidates tumor burden in IDH-mutated gliomas. Neuro Oncol 2022;24:78-87. |
| 55. | Plaza M, Gatignol P, Leroy M, Duffau H. Speaking without Broca's area after tumor resection. Neurocase 2009;15:294-310. |
| 56. | Sarubbo S, Le Bars E, Moritz-Gasser S, Duffau H. Complete recovery after surgical resection of left Wernicke's area in awake patient: A brain stimulation and functional MRI study. Neurosurg Rev 2012;35:287-92. |
| 57. | Duffau H, Capelle L. Functional recuperation following lesions of the primary somatosensory fields. Study of compensatory mechanisms. Neurochirurgie 2001;47:557-63. |
| 58. | Duffau H. Diffuse Low-Grade Gliomas in Adults. New York: Springer; 2017. |
| 59. | Lin Y, Zhang K, Li S, Li S, Jin J, Jin F, et al. Relationship between perisylvian essential language sites and arcuate fasciculus in the left hemisphere of healthy adults. Neurosci Bull 2017;33:616-26. |
| 60. | Picart T, Herbet G, Moritz-Gasser S, Duffau H. Iterative surgical resections of diffuse glioma with awake mapping: How to deal with cortical plasticity and connectomal constraints? Neurosurgery 2019;85:105-16. |
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
[Table 1], [Table 2]
|
Search Pubmed for