Surgery of gliomas in eloquent areas: from brain hodotopy and plasticity to functional neurooncology
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.
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.
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.
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.
✓ 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.
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.
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.
Fadi Ghareeb and Hugues Duffau
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.
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.
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).
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.
Eduardo Santamaria Carvalhal Ribas and Hugues Duffau
Five percent of the general population has olfactory or gustatory disorders, although most do not complain about it. However, in some cases, these symptoms can be disabling and may affect quality of life. Anosmia was reported as a possible complication following head injury and neurosurgical procedures, particularly after the resection of tumors located in the anterior fossa and the treatment of aneurysms in the anterior circulation. Nonetheless, in all of these situations, olfactory dysfunction could be explained by damage to the peripheral olfactory system.
Here, the authors report a case of complete anosmia associated with ageusia following awake resection of a low-grade glioma involving the left temporoinsular region, with no recovery during a follow-up of 3 years. The frontal lobe was not retracted, and the olfactory tract was not visualized during surgery; therefore, postoperative anosmia and ageusia are likely explained by damage to the cortex and central pathways responsible for these senses. The authors suggest that the patient might have had a subclinical right hemianosmia before surgery, which is a common condition. After resection of the central structures critical for smell and taste processing in the left hemisphere, the patient could have finally had bilateral and complete olfactory and gustatory loss.
This is the first known report of permanent anosmia and ageusia following glioma surgery. Because these symptoms might have been underestimated, more attention should be devoted to olfaction and taste, especially with regard to possible subclinical preoperative deficit.
Tej D. Azad and Hugues Duffau
The optimal surgical management of gliomas requires a balance between surgical cytoreduction and preservation of neurological function. Preoperative functional neuroimaging, such as functional MRI (fMRI) and diffusion tensor imaging (DTI), has emerged as a possible tool to inform patient selection and surgical planning. However, evidence that preoperative fMRI or DTI improves extent of resection, limits neurological morbidity, and broadens surgical indications in classically eloquent areas is lacking. In this review, the authors describe facets of functional neuroimaging techniques that may limit their impact on neurosurgical oncology and critically evaluate the evidence supporting fMRI and DTI for patient selection and operative planning in glioma surgery. The authors also propose alternative applications for functional neuroimaging in the care of glioma patients.
Santiago Gil-Robles and Hugues Duffau
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.
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.
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.
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.