✓ Cortical control of micturition and continence remains poorly understood. The authors report two cases of patients who presented with prolonged urinary disturbances after resection of a brain glioma. Accurate anatomofunctional correlations determined using postoperative magnetic resonance imaging support the following: 1) the implication of the posterior portion of the right anterior cingulate gyrus in the perception of bladder sensation and maintenance of continence; 2) the involvement of the right anterior insula in bladder relaxation; and 3) the role of the right inferior frontal cortex in the decision concerning whether to initiate a micturition. On the basis of these results, a preliminary model of a cortical network associated with micturition and continence is proposed.
Hugues Duffau and Laurent Capelle
Hugues Duffau, Dominique Denvil and Laurent Capelle
Object. Despite the high frequency of striatal lesions, the rate of movement disorders reported in the literature is lower than expected (< 10%). To maximize the extent of resection in low-grade gliomas invading the right striatum, the authors performed a striatal resection in a series of 14 patients, observed the lack of movement disorders following these procedures, and discuss herein the mechanisms likely to explain these findings.
Methods. Fourteen patients harboring a low-grade glioma that was infiltrating the right nondominant striatum, and in whom the results of neurological examination were normal, underwent surgery in which intraoperative electrical mapping was used, allowing the identification of pyramidal pathways. The striatum was resected in all procedures, and corticospinal tracts were systematically detected and preserved. Ten patients presented with a transient postoperative motor deficit, and nine with a loss of interest and affect. These symptoms all resolved within 3 months, except for one case of persistent hemiparesis. No postoperative movement disorder was noted, even transitorily. All resections were categorized as either total or subtotal on control magnetic resonance images.
Conclusions. These findings show that the nondominant striatum can be removed in cases of glioma invasion without inducing even transitory movement disorders. This phenomenon could be explained by the combined resection of the two classes of striatal neurons, an associated pallidal and thalamocortical resection, or a compensatory recruitment of parallel networks. Thus, these results may allow the surgeon to maximize the extent of removal of low-grade gliomas involving basal ganglia. Striatal resection may induce transient hemiparesis and “athymhormic syndrome,” however, necessitating that the patient be clearly informed before surgery.
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.
Hugues Duffau, Peggy Gatignol, Emmanuel Mandonnet, Laurent Capelle and Luc Taillandier
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.
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.
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.
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.
Review of 20 cases
Alain Pierre-Kahn, Laurent Capelle, Raja Brauner, Christian Sainte-Rose, Dominique Renier, Raphaël Rappaport and Jean-François Hirsch
✓ The clinical presentation and treatment of suprasellar arachnoid cysts remain controversial. The authors review 20 cases treated at their institution and 86 cases from the literature reported in sufficient detail for analysis. The high frequency of endocrinological disorders, which not only persist following treatment but may also develop years later despite the satisfactory decrease in volume of the cyst, are emphasized and documented. The difficulties of management are discussed, including: subfrontal approaches to these cysts; removal and/or marsupialization of the cysts, procedures that are frequently dangerous and ineffective; and ventricular shunting which often leads to a paradoxical increase in the size of the cysts. The authors emphasize the advantages of percutaneous ventriculocystostomy, which is a simple, benign, and efficacious procedure.
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.
Delphine Leclercq, Hugues Duffau, Christine Delmaire, Laurent Capelle, Peggy Gatignol, Mathieu Ducros, Jacques Chiras and Stéphane Lehéricy
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.
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.
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.
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.
Mitchel S. Berger
Hugues Duffau, Manuel Lopes, Vesna Janosevic, Jean-Pierre Sichez, Thierry Faillot, Laurent Capelle, Mounir Ismaïl, Ahmad Bitar, François Arthuis and Denis Fohanno
Object. In this study the authors sought to estimate the frequency, seriousness, and delay of rebleeding in a homogeneous series of 20 patients whom they treated between May 1987 and May 1997 for arteriovenous fistulas (AVFs) that were revealed by intracranial hemorrhage (ICH). The natural history of intracranial dural AVFs remains obscure. In many studies attempts have been made to evaluate the risk of spontaneous hemorrhage, especially as a function of the pattern of venous drainage: a higher occurrence of bleeding was reported in AVFs with retrograde cortical venous drainage, with an overall estimated rate of 1.8% per year in the largest series in the literature. However, very few studies have been designed to establish the risk of rebleeding, an omission that the authors seek to remedy.
Methods. Presenting symptoms in the 20 patients (17 men and three women, mean age 54 years) were acute headache in 12 patients (60%), acute neurological deficit in eight (40%), loss of consciousness in five (25%), and generalized seizures in one (5%). Results of the clinical examination were normal in five patients and demonstrated a neurological deficit in 12 and coma in three. Computerized tomography scanning revealed intracranial bleeding in all cases (15 intraparenchymal hematomas, three subarachnoid hemorrhages, and two subdural hematomas). A diagnosis of AVF was made with the aid of angiographic studies in 19 patients, whereas it was a perioperative discovery in the remaining patient. There were 12 Type III and eight Type IV AVFs according to the revised classification of Djindjian and Merland, which meant that all AVFs in this study had retrograde cortical venous drainage. The mean duration between the first hemorrhage and treatment was 20 days. Seven patients (35%) presented with acute worsening during this delay due to radiologically proven early rebleeding. Treatment consisted of surgery alone in 10 patients, combined embolization and surgery in eight, embolization only in one, and stereotactic radiosurgery in one. Three patients died, one worsened, and in 16 (80%) neurological status improved, with 15 of 16 AVFs totally occluded on repeated angiographic studies (median follow up 10 months).
Conclusions. The authors found that AVFs with retrograde cortical venous drainage present a high risk of early rebleeding (35% within 2 weeks after the first hemorrhage), with graver consequences than the first hemorrhage. They therefore advocate complete and early treatment in all cases of AVF with cortical venous drainage revealed by an ICH.
Stéphane Lehéricy, Hugues Duffau, Philippe Cornu, Laurent Capelle, Bernard Pidoux, Alexandre Carpentier, Stéphanie Auliac, Stèphane Clemenceau, Jean-Pierre Sichez, Ahmed Bitar, Charles-Ambroise Valery, Remy Van Effenterre, Thierry Faillot, Abbas Srour, Denis Fohanno, Jacques Philippon, Denis Le Bihan and Claude Marsault
Object. The goal of this study was to determine the somatotopical structure—function relationships of the primary motor cortex in individual patients by using functional magnetic resonance (fMR) imaging. This was done to assess whether there is a displacement of functional areas compared with anatomical landmarks in patients harboring brain tumors close to the central region, and to validate these findings with intraoperative cortical stimulation.
Methods. One hundred twenty hemispheres in 60 patients were studied by obtaining blood oxygen level—dependent fMR images in patients while they performed movements of the foot, hand, and face on both sides. There was a good correspondence between anatomical landmarks in the deep portion of the central sulcus on axial slices and the somatotopical organization of primary motor areas. Pixels activated during hand movements were centered on a small characteristic digitation; those activated during movements in the face and foot areas were located in the lower portion of the central sulcus (lateral to the hand area) and around the termination of the central sulcus, respectively. In diseased hemispheres, signal-intensity changes were still observed in the projection of the expected anatomical area. The fMR imaging data mapped intraoperative electrical stimulation in 92% of positive sites.
Conclusions. There was a high correspondence between the somatotopical anatomy and function in the central sulcus, which was similar in normal and diseased hemispheres. The fMR imaging and electrical stimulation data were highly concordant. These findings may enable the neurosurgeon to locate primary motor areas more easily during surgery.