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Yordanka N. Yordanova, Sylvie Moritz-Gasser and Hugues Duffau

Object

It has been demonstrated that an extensive resection (total or subtotal) may significantly increase the overall survival in patients with WHO Grade II gliomas (low-grade gliomas [LGGs]). Yet, recent data have shown that conventional MR imaging underestimates the spatial extent of LGG, since tumor cells were found up to 20 mm around MR imaging abnormalities. Thus, it was hypothesized that an extended resection with a margin beyond MR imaging–defined abnormalities—a “supratotal” resection—might improve the outcome of LGG. However, because of the frequent location of LGG within “eloquent” brain areas, it is often difficult to achieve such a supratotal resection. This could nevertheless be possible when LGGs involve “noneloquent” areas, even in the left dominant hemisphere. The authors report on their use of awake electrical mapping to tailor the resection according to functional boundaries, that is, to pursue the resection beyond MR imaging–defined abnormalities, until corticosubcortical eloquent structures are encountered. Their aim was to apply this reliable surgical technique to LGGs located not within eloquent areas but distant from eloquent areas, to take a margin around the LGG visible on MR imaging while preserving brain function.

Methods

Fifteen right-handed patients with a total of 17 tumors underwent resection of WHO Grade II gliomas involving nonfunctional areas within the left dominant hemisphere. In all patients, seizures were the initial manifestation of the tumors. Awake surgery with intraoperative electrostimulation was performed in all cases. The resection was continued until the surgeon reached cortical and subcortical areas crucial for brain function, especially language, as defined by the intrasurgical electrical mapping. The extent of resection was evaluated on postoperative FLAIR-weighted MR images.

Results

Despite transient neurological worsening in 60% of cases, all patients recovered and returned to a normal life. Seizure control was obtained in all patients with a decrease of antiepileptic drug therapy. Postoperative MR imaging showed that total resection was achieved in all 17 tumors and supratotal resection in 15. The average volume of the postoperative cavity (36.8 cm3) was significantly larger than the mean preoperative tumor volume (26.6 cm3) (p = 0.009). Neuropathological examination confirmed the diagnosis of WHO Grade II glioma in all cases. The mean duration of postoperative follow-up was 35.7 months (range 6–135 months). Only 4 of 15 patients experienced recurrence (without anaplastic transformation); the average time to recurrence in these cases was 38 months; radiotherapy was performed 6 years after the relapse in 1 case; no other patients received any adjuvant treatment. This series was compared with a control group of 29 patients who had “only” complete resection: anaplastic transformation was observed in 7 cases in the control group but not in any case in the series of patients who underwent supracomplete resection (p = 0.037). Furthermore, adjuvant treatment was administered in 10 patients in the control group compared with 1 patient who underwent supracomplete resection (p = 0.043).

Conclusions

These findings support the usefulness of awake surgery with intraoperative functional (language) mapping with the attempt to perform supratotal resection of LGGs involving noneloquent areas in the left hemisphere. Indeed, the extent of resection was significantly increased in all cases but 2, with no additional permanent deficit and with control of seizures in all patients. The goal of supracomplete resection is currently to delay the anaplastic transformation, even if it does not (yet) enable a cure.

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Sylvie Moritz-Gasser and Hugues Duffau

This 47-year-old, right-handed bilingual (French and English) man underwent awake surgery for a glioma in the left dominant posterior temporal lobe. During intraoperative picture naming, direct electrostimulation of a discrete cortical area within the posterior part of the superior temporal sulcus elicited an involuntary language switching (French to English). Moreover, during tumor resection, subcortical electrical mapping again generated reproducible language switching (French to English) when stimulating the superior longitudinal fasciculus. After transient immediately postoperative worsening, the patient recovered normal language performance. Both 7 days and 2 months later, however, another language switching episode (French to English) was observed during a naming task. Thus, both intraoperative mapping and transient postsurgical disturbances support involvement of the left dominant posterior temporal area and the superior longitudinal fasciculus in language switching. Interestingly, this pathway is known to connect the posterosuperior temporal gyrus to the Broca center, a region the authors have described as inducing possible switching on stimulation. Therefore, the authors suggest the existence of a large-scale distributed network subserving language switching. Such knowledge may have important clinical implications for the surgical care of a bilingual patient harboring a lesion in the left hemisphere.

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Guillaume Gras-Combe, Sylvie Moritz-Gasser, Guillaume Herbet and Hugues Duffau

Object

Preservation of the visual field in glioma surgery, especially avoidance of hemianopia, is crucial for patients' quality of life, particularly for driving. Recent studies used tractography or cortical occipital stimulation to try to avoid visual deficit. However, optic radiations have not been directly mapped intraoperatively. The authors present, for the first time to their knowledge, a consecutive series of awake surgeries for cerebral glioma with intrasurgical identification and preservation of visual pathways using subcortical electrical mapping.

Methods

Fourteen patients underwent awake resection of a glioma (1 WHO Grade I, 11 WHO Grade II, 2 WHO Grade III) involving the optic radiations. The patients had no presurgical visual field deficit. Intraoperatively, a picture-naming task was used, with presentation of 2 objects situated diagonally on a screen divided into 4 quadrants. An image was presented in the quadrant to be saved and another image was presented in the opposite quadrant. Direct subcortical electrostimulation was repeatedly performed without the patient's knowledge, until optic radiations were identified (transient visual disturbances). All patients underwent an objective visual field assessment 3 months after surgery.

Results

All patients experienced visual symptoms during stimulation. These disturbances led the authors to stop the tumor resection at that level. Postoperatively, only 1 patient had a permanent hemianopia, despite an expected quadrantanopia in 12 cases. The mean extent of resection was 93.6% (range 85%–100%).

Conclusions

Online identification of optic radiations by direct subcortical electrostimulation is a reliable and effective method to avoid permanent hemianopia in surgery for gliomas involving visual pathways.

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Hugues Duffau, Sylvie Moritz-Gasser and Peggy Gatignol

Object

Despite the report of recent experiences of insular surgery in the past decade, there has been no series specifically dedicated to studying functional outcome following resection of insular WHO Grade II gliomas involving the dominant hemisphere, in patients with no or only mild preoperative language deficit. In this article, the authors analyze the contribution of awake mapping for preservation of brain function, especially language, in a homogeneous series of 24 patients who underwent surgery for insular Grade II gliomas within the dominant insular lobe.

Methods

Twenty-four patients underwent surgery for an insular Grade II glioma involving the dominant hemisphere (22 left, 2 right), revealed by seizures in all but 1 case. The preoperative neurological examination result was normal in 17 patients (71%), whereas 7 patients presented with language disorders detected using an accurate language assessment performed by a speech therapist. All surgeries were performed on awake patients utilizing intra-operative language mapping involving cortical and subcortical stimulation.

Results

There were no intrasurgical complications or postsurgical sensorimotor deficits. Despite an immediate postoperative language worsening in 12 cases (50%), all patients recovered to a normal status within 3 months, and 6 cases even improved in comparison with their preoperative examination results. The 24 patients returned to normal social and professional lives. Moreover, the surgery had a favorable impact on epilepsy in all but 4 cases (83%). On control MR imaging, 62.5% of resections were total or subtotal. Three patients underwent a second or third awake surgery, with no additional deficit. All but 2 patients (92%) are alive after a mean follow-up of 3 years (range 3–133 months).

Conclusions

Although insular surgery was long believed to be too risky, the present results show that the rate of permanent deficit, especially dysphasia, following resection of Grade II gliomas involving the dominant insula has been dramatically reduced (none in this patient series), thanks to the systematic use of intraoperative awake mapping, even in cases of repeated operations. Furthermore, patient quality of life may be improved due to a decrease of epilepsy after surgery. Thus, the authors suggest systematically considering resection when an insular Grade II glioma is diagnosed after seizures in a patient with no or mild deficit, even a glioma invading the dominant hemisphere.

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Hugues Duffau, Sylvie Moritz-Gasser and Peggy Gatignol

Object

Despite the report of recent experiences of insular surgery in the past decade, there has been no series specifically dedicated to studying functional outcome following resection of insular WHO Grade II gliomas involving the dominant hemisphere, in patients with no or only mild preoperative language deficit. In this article, the authors analyze the contribution of awake mapping for preservation of brain function, especially language, in a homogeneous series of 24 patients who underwent surgery for insular Grade II gliomas within the dominant insular lobe.

Methods

Twenty-four patients underwent surgery for an insular Grade II glioma involving the dominant hemisphere (22 left, 2 right), revealed by seizures in all but 1 case. The preoperative neurological examination result was normal in 17 patients (71%), whereas 7 patients presented with language disorders detected using an accurate language assessment performed by a speech therapist. All surgeries were performed on awake patients utilizing intra-operative language mapping involving cortical and subcortical stimulation.

Results

There were no intrasurgical complications or postsurgical sensorimotor deficits. Despite an immediate postoperative language worsening in 12 cases (50%), all patients recovered to a normal status within 3 months, and 6 cases even improved in comparison with their preoperative examination results. The 24 patients returned to normal social and professional lives. Moreover, the surgery had a favorable impact on epilepsy in all but 4 cases (83%). On control MR imaging, 62.5% of resections were total or subtotal. Three patients underwent a second or third awake surgery, with no additional deficit. All but 2 patients (92%) are alive after a mean follow-up of 3 years (range 3–133 months).

Conclusions

Although insular surgery was long believed to be too risky, the present results show that the rate of permanent deficit, especially dysphasia, following resection of Grade II gliomas involving the dominant insula has been dramatically reduced (none in this patient series), thanks to the systematic use of intraoperative awake mapping, even in cases of repeated operations. Furthermore, patient quality of life may be improved due to a decrease of epilepsy after surgery. Thus, the authors suggest systematically considering resection when an insular Grade II glioma is diagnosed after seizures in a patient with no or mild deficit, even a glioma invading the dominant hemisphere.

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Emilie Chan-Seng, Sylvie Moritz-Gasser and Hugues Duffau

Object

Preserving function while optimizing the extent of resection is the main goal in surgery for diffuse low-grade glioma (DLGG). This is particularly relevant for DLGG involving the sagittal stratum (SS), where damage can have severe consequences. Indeed, this structure is a major crossroad in which several important fascicles run. Thus, its complex functional anatomy is still poorly understood. Subcortical electrical stimulation during awake surgery provides a unique opportunity to investigate white matter pathways. This study reports the findings on anatomofunctional correlations evoked by stimulation during resection for gliomas involving the left SS. Surgical outcomes are also detailed.

Methods

The authors performed a review of patients who underwent awake surgery for histopathologically confirmed WHO Grade II glioma involving the left SS in the neurosurgery department between August 2008 and August 2012. Information regarding clinicoradiological features, surgical procedures, and outcomes was collected and analyzed. Intraoperative electrostimulation was used to map the eloquent structures within the SS.

Results

Eight consecutive patients were included in this study. There were 6 men and 2 women, whose mean age was 41.7 years (range 32–61 years). Diagnosis was made because of seizures in 7 cases and slight language disorders in 1 case. After cortical mapping, subcortical stimulation detected functional fibers running in the SS in all patients: semantic paraphasia was generated by stimulating the inferior frontooccipital fascicle in 8 cases; alexia was elicited by stimulating the inferior longitudinal fascicle in 3 cases; visual disorders were induced by stimulating the optic radiations in 5 cases. Moreover, in front of the SS, phonemic paraphasia was evoked by stimulating the temporal part of the arcuate fascicle in 5 patients. The resection was stopped according to these functional limits in the 8 patients. After a transient postsurgical worsening, all patients recovered to normal results on examination, except for the persistence of a right superior quadrantanopia in 5 cases, with no consequences for quality of life. The 8 patients returned to a normal social and professional life. Total or subtotal resection was achieved in all cases but one.

Conclusions

The authors suggest that the use of intrasurgical electrical mapping of the white matter pathways in awake patients opens the door to extensive resection of DLGG within the left SS while preserving the quality of life. Further anatomical, clinical, radiological, and electrophysiological studies are needed for a better understanding of the functional anatomy of this complex region.

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Alejandro Fernández Coello, Sylvie Moritz-Gasser, Juan Martino, Matteo Martinoni, Ryosuke Matsuda and Hugues Duffau

Intraoperative electrical brain mapping is currently the most reliable method to identify eloquent cortical and subcortical structures at the individual level and to optimize the extent of resection of intrinsic brain tumors. The technique allows the preservation of quality of life, not only allowing avoidance of severe neurological deficits but also facilitating preservation of high neurocognitive functions. To accomplish this goal, however, it is crucial to optimize the selection of appropriate intraoperative tasks, given the limited intrasurgical awake time frame. In this review, the authors' aim was to propose specific parameters that could be used to build a personalized protocol for each patient. They have focused on lesion location and relationships with functional networks to guide selection of intrasurgical tasks in an effort to increase reproducibility among neurooncological centers.

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Guillaume Herbet, Gilles Lafargue, Fabien Almairac, Sylvie Moritz-Gasser, François Bonnetblanc and Hugues Duffau

The authors report the first case of a strikingly unusual speech impairment evoked by intraoperative electrostimulation in a 36-year-old right-handed patient, a well-trained singer, who underwent awake surgery for a right fronto-temporo-insular low-grade glioma. Functionally disrupting the pars opercularis of the right inferior frontal gyrus led the patient to automatically switch from a speaking to a singing mode of language production. Given the central role of the right pars opercularis in the inhibitory control network, the authors propose that this finding may be interpreted as possible evidence for a competitive and independent neurocognitive subnetwork devoted to the melodically intoned articulation of words (normal language-based vs singing-based) in subjects with high expertise. From a more clinical perspective, such data may have implications for awake neurosurgery, especially to preserve the quality of life for singers.

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Igor Lima Maldonado, Sylvie Moritz-Gasser, Nicolas Menjot de Champfleur, Luc Bertram, Gérard Moulinié and Hugues Duffau

Object

Surgery in the left dominant inferior parietal lobule (IPL) is challenging because of a high density of somatosensory and language structures, both in the cortex and white matter. In the present study, on the basis of the results provided by direct cerebral stimulation in awake patients, the authors revisit the anatomofunctional aspects of surgery within the left IPL.

Methods

Fourteen consecutive patients underwent awake craniotomy for a glioma involving the left IPL. Intraoperative motor, sensory, and language mapping was performed before and during the tumor removal, at both the cortical and subcortical levels, to optimize the extent of resection, which was determined based on functional boundaries. Anatomofunctional correlations were performed by combining the results of intraoperative mapping and those provided by pre- and postoperative MR imaging.

Results

At the cortical level, the primary somatosensory area (retrocentral gyrus) limited the resection anteriorly in all cases, at least partially. Less frequently, speech arrest or articulatory problems were observed within the parietal operculum (4 cases). The lateral limit was determined by language sites that were variably distributed. Anomia was the most frequent response (9 cases) at the posterior third of the superior (and/or middle) temporal gyrus. Posteriorly, less reproducible reorganized language sites were seldom observed in the posterior portion of the angular gyrus (2 cases). At the subcortical level, in addition to somatosensory responses due to stimulation of the thalamocortical pathways, articulatory disturbances were induced by stimulation of white matter in the anterior and lateral part of the surgical cavity (11 cases). This tract anatomically corresponds to the horizontal portion of the lateral segment of the superior longitudinal fascicle (SLF III). Deeper and superiorly, phonemic paraphasia was the main language disturbance (12 cases), elicited by stimulation of the posterosuperior portion of the arcuate fascicle. All these eloquent structures were surgically preserved. Despite slight cognitive disorders (working memory, writing, or calculation) in 6 cases, no patient retained a severe or a moderate postoperative deficit (except one with right hemianopia [mean follow-up 41.8 months]). Resection was total or near total in 9 patients and partial in 3 cases.

Conclusions

To the authors' knowledge, this is the first series dedicated to the surgery of gliomas involving the left IPL. Interestingly, a certain degree of interindividual variability was observed in the distribution of the cortical maps, especially for language. Therefore, it is suggested that no rigid pattern of resection can be considered within the left IPL, and that surgery in this region should be performed in awake patients to adapt the tumor removal to individual functional limits. Nonetheless, several landmarks have been regularly identified, especially at the subcortical levels (SLF III and arcuate fascicle); a better knowledge of these functional tracts could be helpful to optimize functional outcomes.

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Matthieu Vassal, Emmanuelle Le Bars, S.T. Sylvie Moritz-Gasser, Nicolas Menjot and Hugues Duffau

Object

Crossed aphasia (aphasia resulting from a right hemispheric lesion among right-handed patients) is rare. The authors describe for the first time transient crossed aphasia elicited by intraoperative electrostimulation of both cortex and white matter pathways in awake patients.

Methods

Three right-handed adults underwent surgery for a right-sided glioma. Because slight language disorders occurred during partial seizures or were identified on preoperative cognitive assessment, with right activations detected on language functional MR imaging in 1 patient, awake craniotomy was performed using intraoperative cortico-subcortical electrical functional mapping.

Results

Transient language disturbances were elicited by stimulating discrete cortical areas (inferior frontal gyrus and posterior part of the superior temporal gyrus) and white matter pathways (inferior frontooccipital fasciculus and arcuate fasciculus). A subtotal resection was achieved in all cases, according to functional boundaries. Postoperatively, 1 patient experienced a transient dysphasia, which resolved after speech rehabilitation, with no permanent deficit.

Conclusions

These original findings highlight the possibility of finding crucial cortico-subcortical language networks in the right hemisphere in a subgroup of atypical right-handed patients. These findings provide new insights into the neural basis of language, by underlining the role of the right inferior occipitofrontal fasciculus in semantics and that of the right arcuate fasciculus in phonology, and by supporting the hypothesis of a mirror organization between the right and left hemispheres. The authors suggest that, in right-handed patients, if language disturbances are detected during seizures or on presurgical neuropsychological assessment, especially when right activations are observed on language functional MR imaging, awake craniotomy with intraoperative language mapping should be considered.