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Introduction

Surgery of gliomas in eloquent areas: from brain hodotopy and plasticity to functional neurooncology

Hugues Duffau

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Hugues Duffau

✓ The goal in this study was to determine if intraoperative electrical stimulation mapping is useful during surgical resection of lesions located in the central region, even in cases of preoperative hemiplegia. This 45-year-old man with a retrocentral metastasis from an embryonal carcinoma of the testis suffered an acute complete hemiplegia after intratumoral bleeding. Emergency surgery was performed with the aid of intraoperative motor mapping despite the preoperative deficit. Cortical stimulations (CSs) elicited motor responses, allowing the detection and hence preservation of the primary motor area during tumor removal. Postoperatively, the patient recovered almost completely within 1 week; the tumor resection was total.

It is possible that CSs give an early and valuable prognostic indicator of motor recovery in cases of complete hemiplegia, at least in patients with acute onset and short duration of the deficit. Consequently, if motor responses can be elicited by CSs, it becomes mandatory for the surgeon to respect the primary motor area despite the preoperative hemiplegia, with the aim of preserving the chances of an eventual recovery.

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Hugues Duffau

Object

Few experiences of insular surgery have been reported. Moreover, there are no large surgical studies with long-term follow-up specifically dedicated to WHO Grade II gliomas involving the insula. In this paper, the author describes a personal consecutive series of 51 cases in which patients underwent surgery for an insular Grade II glioma. On the basis of the functional and oncological results, advances and limitations of this challenging surgery are discussed.

Methods

Fifty-one patients harboring an insular Grade II glioma (revealed by seizures in 50 cases) underwent surgery. Findings on preoperative neurological examination were normal in 45 patients (88%). All surgeries were conducted under cortico-subcortical stimulation, and in the case of 16 patients while awake.

Results

Despite an immediate postoperative worsening in 30 cases (59%), the condition of all but 2 patients (96%) returned to baseline or better. Postoperative MR imaging demonstrated that 77% of resections were total or subtotal. Ten patients underwent a second or third surgery, with no additional deficit. Forty-two patients (82%) are alive with a median follow-up of 4 years.

Conclusions

This is the largest reported experience with insular Grade II glioma surgery. The better knowledge of the insular pathophysiology and the use of intraoperative functional mapping allow the risk of permanent deficit to be minimized (and even enable improvement in quality of life) while increasing the extent of resection and thus the impact on the course of the disease. Therefore, surgical removal must always be considered for insular Grade II glioma. However, this surgery remains challenging, especially within the anterior perforating substance and the posterior part of the (dominant) insula. Additional surgery can be suggested in cases in which the first resection is not complete.

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Hugues Duffau and Laurent Capelle

✓ 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.

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Thiébaud Picart and Hugues Duffau

A 30-year-old right-handed female medical doctor experienced generalized seizures. MRI showed a left operculo-insular low-grade glioma. Awake resection was proposed. During the cortical mapping, counting and naming task combined with right upper limb movement enabled the identification of the ventral premotor cortex and negative motors areas. The so-called Broca’s area was not eloquent. Subpial dissection was performed by avoiding coagulation until the inferior fronto-occipital fasciculus and the junction between the output projection fibers and the anterior part of the superior longitudinal fasciculus III were reached. The patient resumed a normal familial and socio-professional life despite the resection of Broca’s area.

The video can be found here: https://youtu.be/OALk0tvctQw.

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Fadi Ghareeb and Hugues Duffau

Object

Beyond its oncological benefit, surgery could improve seizure control in paralimbic frontotemporoinsular or temporoinsular WHO Grade II gliomas generating intractable seizures. However, no studies have examined the impact of hippocampal resection on chronic epilepsy when the hippocampus is not invaded by Grade II gliomas. Here, the authors compared the epileptological outcomes and return to work in 2 groups of patients who underwent surgery with or without hippocampectomy for paralimbic Grade II gliomas eliciting intractable epilepsy despite no tumoral involvement of the hippocampus.

Methods

Surgery was performed in 15 consecutive patients who were unable to work (median Karnofsky Performance Scale [KPS] Score 70) because of refractory epilepsy due to paralimbic Grade II gliomas that were not invading the hippocampus. In Group A (8 patients), the hippocampus was preserved. In Group B (7 patients), glioma removal was associated with hippocampectomy.

Results

No patient died or suffered a permanent deficit after surgery. Postoperatively, in Group A, no patients were seizure free (4 patients were in Engel Class II and 4 were in Class III). In Group B, all 7 patients were seizure free (Class I) (p = 0.02). Only 62.5% of patients returned to work in Group A, whereas all patients are working full time in Group B. The postsurgical median KPS score was 85 in Group A, that is, not significantly improved in comparison with the preoperative score, while the postsurgical median KPS was 95 in Group B, that is, significantly improved in comparison with the preoperative score (p = 0.03).

Conclusions

The authors' data support, for the first time, the significant impact of hippocampectomy in patients with intractable epilepsy generated by a paralimbic Grade II glioma, even if it does not invade the hippocampus. Hippocampal resection allowed seizure control in all patients, with an improvement in KPS scores, since all patients resumed their social and professional activities. Thus, the authors suggest performing a resection of the nontumoral hippocampus in addition to resection of the tumor in patients with refractory epilepsy due to paralimbic Grade II gliomas.

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Santiago Gil-Robles and Hugues Duffau

Object

Recent surgical studies have demonstrated that the extent of resection is significantly correlated with median survival in WHO Grade II gliomas. Consequently, thanks to advances in intraoperative functional mapping, the authors questioned whether it is actually necessary to leave a “security” margin around eloquent structures.

Methods

The authors first reviewed the classic literature, especially that based on epilepsy surgery and functional neuroimaging techniques, which led them to propose the rule of a security margin. Second, they detailed new developments in the field of intrasurgical electrical mapping, especially with regard to subcortical stimulation of the projection and long-distance association pathways. On the basis of these advances, the removal of gliomas according to functional boundaries has recently been suggested, with no margin around eloquent structures.

Results

Comparative results showed that the rate of permanent deficit was similar with or without a security margin, that is, < 2%. However, a higher rate of transient neurological worsening in the immediate postsurgical period was associated with the absence of a margin, with recovery following adapted rehabilitation. On the other hand, the extent of resection was in essence improved with no margin.

Conclusions

This no-margin technique, based on the subpial dissection, and the repetition of both cortical and subcortical stimulation to preserve eloquent cortex as well as the white matter tracts (U-fibers, projection pathways, and long-distance connectivity) allow optimization of the extent of resection while preserving the quality of life (despite transitory impairment) thanks to mechanisms of brain plasticity.

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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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Alessandro De Benedictis, Silvio Sarubbo, and Hugues Duffau

Object

Recent neuroimaging and surgical results support the crucial role of white matter in mediating motor and higher-level processing within the frontal lobe, while suggesting the limited compensatory capacity after damage to subcortical structures. Consequently, an accurate knowledge of the anatomofunctional organization of the pathways running within this region is mandatory for planning safe and effective surgical approaches to different diseases. The aim of this dissection study was to improve the neurosurgeon's awareness of the subcortical anatomofunctional architecture for a lateral approach to the frontal region, to optimize both resection and postoperative outcome.

Methods

Ten human hemispheres (5 left, 5 right) were dissected according to the Klingler technique. Proceeding lateromedially, the main association and projection tracts as well as the deeper basal structures were identified. The authors describe the anatomy and the relationships among the exposed structures in both a systematic and topographical surgical perspective. Structural results were also correlated to the functional responses obtained during resections of infiltrative frontal tumors guided by direct cortico-subcortical electrostimulation with patients in the awake condition.

Results

The eloquent boundaries crucial for a safe frontal lobectomy or an extensive lesionectomy are as follows: 1) the motor cortex; 2) the pyramidal tract and premotor fibers in the posterior and posteromedial part of the surgical field; 3) the inferior frontooccipital fascicle and the superior longitudinal fascicle posterolaterally; and 4) underneath the inferior frontal gyrus, the head of the caudate nucleus, and the tip of the frontal horn of the lateral ventricle in the depth.

Conclusions

Optimization of results following brain surgery, especially within the frontal lobe, requires a perfect knowledge of functional anatomy, not only at the cortical level but also with regard to subcortical white matter connectivity.