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Hugues Duffau, Ihab Khalil, Peggy Gatignol, Dominique Denvil, and Laurent Capelle

Object. Although still controversial, many authors currently advocate extensive resection in the treatment of low-grade gliomas (LGGs). Because these tumors usually migrate along white matter pathways, the corpus callosum is often invaded. Nevertheless, there is evidently no specific study featuring resection of the corpus callosum infiltrated by glioma, despite abundant literature concerning callosotomy in epilepsy surgery or transcallosal ventricular approaches. The aim of this paper was to analyze functional outcome following removal of corpus callosum invaded by LGG and to analyze the impact of this callosectomy on the quality of resection.

Methods. Between 1996 and 2002, a total of 32 patients harboring an LGG involving part of the corpus callosum and having no or only a mild preoperative deficit underwent surgery aided by intraoperative electrical mapping to preserve eloquent structures identified on stimulation and to perform the most extensive resection possible.

Preoperatively, no clinical response was elicited on stimulation of the corpus callosum; thus, the part of this structure that was invaded by LGG was removed. Despite immediate postoperative neurological worsening, all patients but one recovered within 3 months and returned to a normal socioprofessional life. The additional callosectomy allowed for nine total resections, 18 subtotal resections, and five partial resections. Furthermore, only two cases of contralateral hemispherical migration occurred during a median follow up of 3 years.

Conclusions. Resection of the corpus callosum infiltrated by glioma improves the quality of tumor removal without increasing the risk of sequelae.

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Santiago Gil Robles, Peggy Gatignol, Stéphane Lehéricy, and Hugues Duffau

Although the goal of surgery for World Health Organization Grade II gliomas is maximal extent of resection, complete tumor removal is not always possible when the glioma involves eloquent areas. The authors propose a multistage surgical approach to highly crucial areas that are classically considered inoperable, enabling optimization of the extent of resection while avoiding permanent cognitive deficits due to induced functional reshaping in the interim between the 2 consecutive operations. To demonstrate such plasticity, the authors used a combination of sequential functional MR imaging and intraoperative electrical stimulation mapping before and during surgeries spaced by several years in 2 patients who each underwent 2 separate resections of Grade II gliomas located in the left dominant premotor area. During several years of follow-up after the first procedure, both patients had unremarkable examination results and normal socioprofessional lives. There was no malignant transformation. Based on their experience with these cases, the authors suggest that in cases of incomplete glioma removal, a second operation before anaplasia should be considered, made possible by brain reorganization after the first operation.

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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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Hugues Duffau, Peggy Gatignol, Emmanuel Mandonnet, Laurent Capelle, and Luc Taillandier

Object

Despite better knowledge of cortical language organization, its subcortical anatomofunctional connectivity remains poorly understood. The authors used intraoperative subcortical stimulation in awake patients undergoing operation for a glioma in the left dominant hemisphere to map the language pathways and to determine the contribution of such a method to surgical results.

Methods

One hundred fifteen patients harboring a World Health Organization Grade II glioma within language areas underwent operation after induction of local anesthesia, using direct electrical stimulation to perform online cortical and subcortical language mapping throughout the resection.

Results

After detection of cortical language sites, the authors identified 1 or several of the following subcortical language pathways in all patients: 1) arcuate fasciculus, eliciting phonemic paraphasia when stimulated; 2) inferior frontooccipital fasciculus, generating semantic paraphasia when stimulated; 3) subcallosal fasciculus, inducing transcortical motor aphasia during stimulation; 4) frontoparietal phonological loop, eliciting speech apraxia during stimulation; and 5) fibers coming from the ventral premotor cortex, inducing anarthria when stimulated. These structures were preserved, representing the limits of the resection. Despite a transient immediate postoperative worsening, all but 2 patients (98%) returned to baseline or better. On control MR imaging, 83% of resections were total or subtotal.

Conclusions

These results represent the largest experience with human subcortical language mapping ever reported. The use of intraoperative cortical and subcortical stimulation gives a unique opportunity to perform an accurate and reliable real-time anatomofunctional study of language connectivity. Such knowledge of the individual organization of language networks enables practitioners to optimize the benefit-to-risk ratio of surgery for Grade II glioma within the left dominant hemisphere.

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Hugues Duffau, Laurent Capelle, Dominique Denvil, Nicole Sichez, Peggy Gatignol, Luc Taillandier, Manuel Lopes, Mary-Christine Mitchell, Sabine Roche, Jean-Charles Muller, Ahmad Bitar, Jean-Pierre Sichez, and Rémy van Effenterre

Object. Although a growing number of authors currently advocate surgery to treat low-grade gliomas, controversy still persists, especially because of the risk of inducing neurological sequelae when the tumor is located within eloquent brain areas. Many researchers performing preoperative neurofunctional imaging and intraoperative electrophysiological methods have recently reported on the usefulness of cortical functional mapping. Despite the frequent involvement of subcortical structures by these gliomas, very few investigators have specifically raised the subject of fiber tracking. The authors in this report describe the importance of mapping cortical and subcortical functional regions by using intraoperative realtime direct electrical stimulations during resection of low-grade gliomas.

Methods. Between 1996 and 2001, 103 patients harboring a corticosubcortical low-grade glioma in an eloquent area, with no or only mild deficit, had undergone surgery during which intraoperative electrical mapping of functional cortical sites and subcortical pathways was performed throughout the procedure.

Both eloquent cortical areas and corresponding white fibers were systematically detected and preserved, thus defining the resection boundaries. Despite an 80% rate of immediate postoperative neurological worsening, 94% of patients recovered their preoperative status within 3 months—10% even improved—and then returned to a normal socioprofessional life. Eighty percent of resections were classified as total or subtotal based on control magnetic resonance images.

Conclusions. The use of functional mapping of the white matter together with cortical mapping allowed the authors to optimize the benefit/risk ratio of surgery of low-grade glioma invading eloquent regions. Given that preoperative fiber tracking with the aid of neuroimaging is not yet validated, we used intraoperative real-time cortical and subcortical stimulations as a valuable adjunct to the other mapping methods.

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Delphine Leclercq, Hugues Duffau, Christine Delmaire, Laurent Capelle, Peggy Gatignol, Mathieu Ducros, Jacques Chiras, and Stéphane Lehéricy

Object

Diffusion tensor (DT) imaging tractography is increasingly used to map fiber tracts in patients with surgical brain lesions to reduce the risk of postoperative functional deficit. There are few validation studies of DT imaging tractography in these patients. The aim of this study was to compare DT imaging tractography of language fiber tracts by using intraoperative subcortical electrical stimulations.

Methods

The authors included 10 patients with low-grade gliomas or dysplasia located in language areas. The MR imaging examination included 3D T1-weighted images for anatomical coregistration, FLAIR, and DT images. Diffusion tensors and fiber tracts were calculated using in-house software. Four tracts were reconstructed in each patient including the arcuate fasciculus, the inferior occipitofrontal fasciculus, and 2 premotor fasciculi (the subcallosal medialis fiber tract and cortical fibers originating from the medial and lateral premotor areas). The authors compared fiber tracts reconstructed using DT imaging with those evidenced using intraoperative subcortical language mapping.

Results

Seventeen (81%) of 21 positive stimulations were concordant with DT imaging fiber bundles (located within 6 mm of a fiber tract). Four positive stimulations were not located in the vicinity of a DT imaging fiber tract. Stimulations of the arcuate fasciculus mostly induced articulatory and phonemic/syntactic disorders and less frequently semantic paraphasias. Stimulations of the inferior occipitofrontal fasciculus induced semantic paraphasias. Stimulations of the premotor-related fasciculi induced dysarthria and articulatory planning deficit.

Conclusions

There was a good correspondence between positive stimulation sites and fiber tracts, suggesting that DT imaging fiber tracking is a reliable technique but not yet optimal to map language tracts in patients with brain lesions. Negative tractography does not rule out the persistence of a fiber tract, especially when invaded by the tumor. Stimulations of the different tracts induced variable language disorders that were specific to each fiber tract.