Subcortical language and non-language mapping in awake brain surgery: the use of multimodal tests

Subcortical language and non-language mapping in awake brain surgery- the use of multimodal tests

Acta Neurochir (2015) 157:577–588

Awake craniotomy is currently considered the gold standard to maximise the extent of resection and to minimise postoperative deficits in patients with supratentorial tumours near eloquent areas. In addition to direct electrical stimulation (DES) of the cortex, intraoperative subcortical mapping is increasingly used as it optimises the benefit-to-risk ratio by decreasing (permanent) postoperative neurological deficits. However, only little attention has been paid to subcortical mapping procedures and especially the tasks to be used.

Methods In this article, language and non-language testing at the subcortical level is described and discussed by means of three right-handed cases with a glioma in the left hemisphere. To assess subcortical functions, a multimodal test named the Quick Mixed Test was developed (QMT). Pre-, intra- and postoperative test results are described and discussed in detail.

Results Based on the analysis of these preliminary observations, a number of clinical recommendations for intraoperative subcortical mapping may be made: (1) the selection of a set of language and non-language tests needs to be tailored according to the functional corticosubcortical regions affected by the tumoral lesion and the patient’s characteristics (job/hobby/daily life activities); (2) language and non-language tests should be presented in a multimodal and alternating way during subcortical stimulation since this approach enables screening various functions simultaneously or in a very short period of time and (3) spontaneous speech is a useful adjunct to standardised tests since it most resembles daily life conversation.

Conclusion Administration of multimodal tests during subcortical DES such as the experimental QMT may facilitate identification of eloquent pathways leading to avoidance of permanent neurological impairments.

New concepts in the management of diffuse low-grade glioma: Proposal of a multistage and individualized therapeutic approach

New concepts in the management of diffuse low-grade glioma- Proposal of a multistage and individualized therapeutic approach

Neuro-Oncology 17(3), 332–342, 2015

Diffuse low-grade glioma grows, migrates along white matter tracts, and progresses to high-grade glioma. Rather than a “wait and see” policy, an aggressive attitude is now recommended, with early surgery as the first therapy. Intraoperative mapping, with maximal resection according to functional boundaries, is associated with a longer overall survival (OS) while minimizing morbidity.

However, most studies have investigated the role of only one specific treatment (surgery, radiotherapy, chemotherapy) without taking a global view of managing the cumulative time while preserving quality of life (QoL) versus time to anaplastic transformation.

Our aim is to switch towards a more holistic concept based upon the anticipation of a personalized and long-term multistage therapeutic approach, with online adaptation of the strategy over the years using feedback from clinical, radiological, and histomolecular monitoring.

This dynamic strategy challenges the traditional approach by proposing earlier therapy, by repeating treatments, and by reversing the classical order of therapies (eg, neoadjuvant chemotherapy when maximal resection is impossible, no early radiotherapy) to improve OS and QoL.

New individualized management strategies should deal with the interactions between the course of this chronic disease, reaction brain remapping, and oncofunctional modulation elicited by serial treatments. This philosophy supports a personalized, functional, and preventive neuro-oncology.

Insular low-grade glioma and postoperative seizure outcome

Surgery for insular low-grade glioma- predictors of postoperative seizure outcome

J Neurosurg 120:12–23, 2014

Although a number of recent studies on the surgical treatment of insular low-grade glioma (LGG) have demonstrated that aggressive resection leads to increased overall patient survival and decreased malignant progression, less attention has been given to the results with respect to tumor-related epilepsy. The aim of this investigation was to evaluate the impact of volumetric, histological, and intraoperative neurophysiological factors on seizure outcome in patients with insular LGG.

Methods. The authors evaluated predictors of seizure outcome with special emphasis on both the extent of tumor resection (EOR) and the tumor’s infiltrative pattern quantified by computing the difference between the preoperative T2- and T1-weighted MR images (DVT2T1) in 52 patients with preoperative drug-resistant epilepsy.

Results. The 12-month postoperative seizure outcome (Engel class) was as follows: seizure free (Class I), 67.31%; rare seizures (Class II), 7.69%; meaningful seizure improvement (Class III), 15.38%; and no improvement or worsening (Class IV), 9.62%. Poor seizure control was more common in patients with a longer preoperative seizure history (p < 0.002) and higher frequency of seizures (p = 0.008). Better seizure control was achieved in cases with EOR ≥ 90% (p < 0.001) and DVT2T1 < 30 cm3 (p < 0.001). In the final model, DVT2T1 proved to be the strongest independent predictor of seizure outcome in insular LGG patients (p < 0.0001).

Conclusions. No or little postoperative seizure improvement occurs mainly in cases with a prevalent infiltrative tumor growth pattern, expressed by high DVT2T1 values, which consequently reflects a smaller EOR.

Tolerance of awake surgery for glioma: a prospective European Low Grade Glioma Network multicenter study

awake surgery for glioma

Acta Neurochir (2013) 155:1301–1308

Gross total removal of glioma is limited by proximity to eloquent brain. Awake surgery allows for intraoperative monitoring to safely identify eloquent regions. However, data on adverse psychological effects induced in these patients is limited.

Objective This study explored patients’ perception of awake surgery for glioma, with special focus on intraoperative pain and anxiety.

Methods This study was conducted at five neurosurgical centers within the European Low Grade Glioma Network. Patients underwent awake surgery for glioma according to the protocol of the individual center. Pain and discomfort were measured during the awake phase. Postoperatively, patients answered a questionnaire on aspects of their operation.

Results One hundred five patients were enrolled. Pain levels on a 10-cm visual analogue scale were 1.3 cm at the beginning, 1.9 cm the middle, and 2.1 cm at the end of awake phase. Levels of anxiety were 2.2 cm, 2.5 cm and 2.6 cm, respectively. Women and patients younger than 60 years exhibited highest mean anxiety levels. The patient questionnaire revealed that the majority of patients feel comfortable with the procedure. Discomfort resulted from head fixation or positioning on the operating table.

Conclusions We demonstrate that awake surgery is well tolerated, as neither intraoperative nor postoperative assessment revealed major disadvantages. Concerning practical lessons learned from this study, we emphasize the importance of minimizing pain and preparing patients thoroughly to reduce anxiety and maximize cooperation. Awake surgery is an excellent treatment modality for brain tumors with very positive perception by patients. Keywords

A Comparison of Language Mapping by Preoperative Navigated Transcranial Magnetic Stimulation and Direct Cortical Stimulation During Awake Surgery

A_Comparison_of_Language_Mapping_by_Preoperative

Neurosurgery 72:808–819, 2013

Navigated transcranial magnetic stimulation (nTMS) is increasingly used in presurgical brain mapping. Preoperative nTMS results correlate well with direct cortical stimulation (DCS) data in the identification of the primary motor cortex. Repetitive nTMS can also be used for mapping of speech-sensitive cortical areas.

OBJECTIVE: The current cohort study compares the safety and effectiveness of preoperative nTMS with DCS mapping during awake surgery for the identification of language areas in patients with left-sided cerebral lesions.

METHODS: Twenty patients with tumors in or close to left-sided language eloquent regions were examined by repetitive nTMS before surgery. During awake surgery, language-eloquent cortex was identified by DCS. nTMS results were compared for accuracy and reliability with regard to DCS by projecting both results into the cortical parcellation system.

RESULTS: Presurgical nTMS maps showed an overall sensitivity of 90.2%, specificity of 23.8%, positive predictive value of 35.6%, and negative predictive value of 83.9% compared with DCS. For the anatomic Broca’s area, the corresponding values were a sensitivity of 100%, specificity of 13.0%, positive predictive value of 56.5%, and negative predictive value of 100%, respectively.

CONCLUSION: Good overall correlation between repetitive nTMS and DCS was observed, particularly with regard to negatively mapped regions. Noninvasive inhibition mapping with nTMS is evolving as a valuable tool for preoperative mapping of language areas. Yet its low specificity in posterior language areas in the current study necessitates further research to refine the methodology.

Awake mapping for resection of cavernous angioma and surrounding gliosis in the left dominant hemisphere

Awake mapping for resection of cavernous angioma and surrounding gliosis in the left dominant hemisphere

J Neurosurg 117:1076–1081, 2012

Maximal resection of symptomatic cavernous angioma (CA), including its surrounding gliosis if possible, has been recommended to minimize the risk of seizures or (re)bleeding. However, despite recent neurosurgical advances, such extensive CA removal is still a challenge in eloquent areas. The authors report a consecutive series of patients who underwent awake surgery for CA within the left dominant hemisphere in which intraoperative cortical– subcortical electrical stimulation was used.

Methods. Nine patients harboring a CA that was revealed by seizures in 6 cases and bleeding in 3 cases underwent resection. All CAs were located in the left dominant hemisphere: 3 temporal, 2 insular, 2 parietal, and 2 in the parietotemporal region. Awake mapping was performed in all cases by using intraoperative cortical–subcortical electrical stimulation and ultrasonography (except in 1 insular CA in which a neuronavigation system was used).

Results. Total removal of the CA was achieved in all patients, with identification and preservation of language and sensory-motor structures. In addition, the pericavernomatous gliosis was removed in 7 cases, according to the functional boundaries provided by intraoperative subcortical stimulation. In 2 cases, subcortical mapping revealed eloquent areas within the surrounding gliosis, which was voluntarily avoided. There was no postsurgical permanent deficit, no rebleeding, and no epilepsy in 7 cases (2 patients had rare seizures in the 1st year or two after surgery, and then complete arrest), with a mean follow-up of 28.5 months (range 3–64 months).

Conclusions. These results suggest that intraoperative cortical–subcortical stimulation in awake patients represents a valuable adjunct to image-guided surgery with the aim of selecting the safer surgical approach for CAs involving eloquent areas. Moreover, such online mapping can be helpful when removing the pericavernomatous gliosis while preserving functional structures, which can persist within the hemosiderin rim. Thus, the authors propose that awake surgery be routinely considered, both to optimize the resection and to improve the quality of life through seizure control and avoidance of (re)bleeding for CAs located in the left dominant hemisphere.

Intermittent General Anesthesia With Controlled Ventilation for Asleep-Awake-Asleep Brain Surgery

Neurosurgery 71:764–772, 2012

Awake brain tumor surgery is a unique opportunity for mapping sensorimotor and cognitive functions, allowing the operator to optimize the resection while preserving the patient’s quality of life. During this type of procedure, active participation of the patient is necessary.

OBJECTIVE: To assess the efficacy and safety of a method of intermittent general anesthesia with controlled ventilation for performing invasive cerebral mapping. METHODS: We report our prospective and observational single-center study with an asleep-awake-asleep protocol. Aspects of feasibility, airway management, timing of each phase, and occurrence of adverse events were detailed.

RESULTS: During a 35-month period, 140 patients underwent resection of a glioma in an eloquent area. During the asleep phases, controlled ventilation with a laryngeal mask was always efficient. Orotracheal intubation was performed for some patients for the second asleep period. The patients remained fully awake for a mean time of 98 minutes. Postural discomfort was reported in 17.8% of cases. There was 1 case of aspiration of gastric contents with a favorable outcome and no mortality.

CONCLUSION: Intermittent general anesthesia with controlled ventilation for this type of neurosurgical procedure remains an anesthesiological challenge. However, the results of this study suggest that it may be feasible, reproducible, and relatively safe in the context of a standardized protocol involving members of both anesthesiology and surgery teams. Such a technique has a great potential to improve the surgical results, from both oncological and functional perspectives.

Awake surgery for incidental WHO grade II gliomas involving eloquent areas

Acta Neurochir (2012) 154:575–584.DOI 10.1007/s00701-011-1216-x
WHO grade II glioma (G2G) is a premalignant tumor, usually revealed by seizures in young patients living normal lives. G2G grows constantly and will inevitably become anaplastic. Surgical resection significantly increases the overall survival by delaying malignant transformation. Recently, a similar natural history was demonstrated in a patient with incidental G2G, with continuous growth and risk of anaplasia. Here, the aim was to study for the first time the functional results and extent of resection in a prospective series of patients who underwent resection for incidental G2G within eloquent areas.
Method G2G involving functional regions in the left dominant hemisphere was incidentally diagnosed in 11 asymptomatic patients. Resection was achieved in all cases after demonstration of a volumetric increase on serial MRIs. Intraoperative awake mapping was performed in the 11 patients.
Findings There were no cases of mortality or permanent postoperative deficit. A subtotal, total or even “supratotal” resection was achieved in the 11 cases, with no partial resections. All patients resumed normal social and professional lives, with no seizures (KPS 100). Due to slow tumor re-growth in three patients with subtotal resection, adjuvant chemotherapy was administrated in two cases and radiotherapy in one. With a mean follow-up of 40 months since surgery, there was no anaplastic transformation.
Conclusion These results show that surgery can be considered in incidental G2G, even in critical areas, with a minimal risk and optimal resection, thanks to intraoperative mapping. Such findings raise the question of an early detection.

Occipital WHO grade II gliomas: oncological, surgical and functional considerations

Acta Neurochir (2011) 153:1907–1917. DOI 10.1007/s00701-011-1125-z

Diffuse WHO grade II glioma (GIIG) involving the occipital lobe is a rare entity. Its surgical resection remains controversial as it implies inducing a permanent visual deficit. For the first time to our knowledge, we report a consecutive surgical series of patients who underwent an occipital lobectomy for an LGG invading visual structures.

Method Six right-handed patients harboring a GIIG revealed by seizures (normal examination except a quadrantanopsia in one case) and located within the occipital lobe (4 left and 2 right tumors) were submitted to surgery. Before making this decision, the benefit-to-risk ratio of the resection was extensively discussed with the patient and his/her family, especially concerning the price to pay to remove the tumor, that is, to voluntarily generate a permanent hemianopsia. All the procedures were performed under awake condition using intraoperative electrostimulation, in order to pursue the resection until sensory-motor and/or language structures were encountered.

Findings An extensive occipital lobectomy was achieved in the six patients, with identification and preservation of sensory-motor pathways in the two cases with a right tumor and detection of language pathways in the four cases with a left tumor. The mean extent of resection was 93% (range: 91–100%). All patients experienced an expected postoperative deficit of the visual field (homonymous hemianopsia). Nonetheless, the six patients resumed a normal social and professional life (KPS at 90 in the 6 cases) with a mean follow-up of 58 months (range: 3–147 months)—with adjuvant treatment in three cases (in addition to a reoperation in two of them).

Conclusions Our findings suggest that, despite a definitive hemianopsia, an extensive surgical resection can be considered in the rare cases of occipital GIIG involving the primary visual structures, with patients able to maintain a normal life—except regarding the medico-legal problem of driving.

Awake surgery for WHO Grade II gliomas within “noneloquent” areas in the left dominant hemisphere: toward a “supratotal” resection

J Neurosurg 115:232–239, 2011. DOI: 10.3171/2011.3.JNS101333

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 FLAIRweighted 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.

Awake Mapping Optimizes the Extent of Resection for Low-Grade Gliomas in Eloquent Areas

Neurosurgery 66:1074-1084, 2010 DOI: 10.1227/01.NEU.0000369514.74284.78

Awake craniotomy with intraoperative electrical mapping is a reliable method to minimize the risk of permanent deficit during surgery for low-grade glioma located within eloquent areas classically considered inoperable. However, it could be argued that preservation of functional sites might lead to a lesser degree of tumor removal. To the best of our knowledge, the extent of resection has never been directly compared between traditional and awake procedures.

OBJECTIVE: We report for the first time a series of patients who underwent 2 consecutive surgeries without and with awake mapping.

METHODS: Nine patients underwent surgery for a low-grade glioma in functional sites under general anesthesia in other institutions. The resection was subtotal in 3 cases and partial in 6 cases. There was a postoperative worsening in 3 cases. We performed a second surgery in the awake condition with intraoperative electrostimulation. The resection was performed according to functional boundaries at both the cortical and subcortical levels.

RESULTS: Postoperative magnetic resonance imaging showed that the resection was complete in 5 cases and subtotal in 4 cases (no partial removal) and that it was improved in all cases compared with the first surgery (P = .04). There was no permanent neurological worsening. Three patients improved compared with the presurgical status. All patients returned to normal professional and social lives.

CONCLUSION: Our results demonstrate that awake surgery, known to preserve the quality of life in patients with low-grade glioma, is also able to significantly improve the extent of resection for lesions located in functional regions.


Awake Surgery for Nonlanguage Mapping

Neurosurgery 66:523-529, 2010 DOI: 10.1227/01.NEU.0000364996.97762.73

During the past decade, numerous reports have supported the contribution  of awake mapping in surgical removal of brain lesions in eloquent areas, with a significant  increase of the extent of resection while minimizing the risk of permanent deficit—and  even improving quality of life.

METHODS: Most of these awake procedures were performed in patients with lesions in  language areas, to avoid postoperative aphasia. Surprisingly, mapping of nonlanguage  functions received less attention, despite the possible consequences of deficits other than  aphasia on daily life. Visuospatial and cognitive deficits are reported after brain surgery,  because of more objective and extensive neuropsychological assessments.

RESULTS AND CONCLUSION: This review provides new insights into the indications of  awake craniotomies for nonlanguage mapping in surgery for lesions in areas not related  to language processing.

Surgical management of World Health Organization Grade II gliomas in eloquent areas: the necessity of preserving a margin around functional structures

Neurosurg Focus 28 (2):E8, 2010. DOI: 10.3171/2009.12.FOCUS09236

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.

Functional outcome after language mapping for insular WHO Grade II gliomas in the dominant hemisphere: experience with 24 patients

Neurosurg Focus 27 (2):E7, 2009
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.