Correlation between localization of supratentorial glioma to the precentral gyrus and difficulty in identification of the motor area during awake craniotomy

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  • 1 Department of Neurosurgery and
  • 2 Faculty of Advanced Techno-Surgery, Tokyo Women’s Medical University, Tokyo, Japan
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OBJECTIVE

Identification of the motor area during awake craniotomy is crucial for preservation of motor function when resecting gliomas located within or close to the motor area or the pyramidal tract. Nevertheless, sometimes the surgeon cannot identify the motor area during awake craniotomy. However, the factors that influence failure to identify the motor area have not been elucidated. The aim of this study was to assess whether tumor localization was correlated with a negative cortical response in motor mapping during awake craniotomy in patients with gliomas located within or close to the motor area or pyramidal tract.

METHODS

Between April 2000 and May 2019 at Tokyo Women’s Medical University, awake craniotomy was performed to preserve motor function in 137 patients with supratentorial glioma. Ninety-one of these patients underwent intraoperative cortical motor mapping for a primary glioma located within or close to the motor area or pyramidal tract and were enrolled in the study. MRI was used to evaluate whether or not the tumors were localized to or involved the precentral gyrus. The authors performed motor functional mapping with electrical stimulation during awake craniotomy and evaluated the correlation between identification of the motor area and various clinical characteristics, including localization to the precentral gyrus.

RESULTS

Thirty-four of the 91 patients had tumors that were localized to the precentral gyrus. The mean extent of resection was 89.4%. Univariate analyses revealed that identification of the motor area correlated significantly with age and localization to the precentral gyrus. Multivariate analyses showed that older age (≥ 45 years), larger tumor volume (> 35.5 cm3), and localization to the precentral gyrus were significantly correlated with failure to identify the motor area (p = 0.0021, 0.0484, and 0.0015, respectively). Localization to the precentral gyrus showed the highest odds ratio (14.135) of all regressors.

CONCLUSIONS

Identification of the motor area can be difficult when a supratentorial glioma is localized to the precentral gyrus. The authors’ findings are important when performing awake craniotomy for glioma located within or close to the motor area or the pyramidal tract. A combination of transcortical motor evoked potential monitoring and awake craniotomy including subcortical motor mapping may be needed for removal of gliomas showing negative responses in the motor area to preserve the motor-related subcortical fibers.

ABBREVIATIONS EOR = extent of resection; MEP = motor evoked potential; MMT = manual muscle testing.

OBJECTIVE

Identification of the motor area during awake craniotomy is crucial for preservation of motor function when resecting gliomas located within or close to the motor area or the pyramidal tract. Nevertheless, sometimes the surgeon cannot identify the motor area during awake craniotomy. However, the factors that influence failure to identify the motor area have not been elucidated. The aim of this study was to assess whether tumor localization was correlated with a negative cortical response in motor mapping during awake craniotomy in patients with gliomas located within or close to the motor area or pyramidal tract.

METHODS

Between April 2000 and May 2019 at Tokyo Women’s Medical University, awake craniotomy was performed to preserve motor function in 137 patients with supratentorial glioma. Ninety-one of these patients underwent intraoperative cortical motor mapping for a primary glioma located within or close to the motor area or pyramidal tract and were enrolled in the study. MRI was used to evaluate whether or not the tumors were localized to or involved the precentral gyrus. The authors performed motor functional mapping with electrical stimulation during awake craniotomy and evaluated the correlation between identification of the motor area and various clinical characteristics, including localization to the precentral gyrus.

RESULTS

Thirty-four of the 91 patients had tumors that were localized to the precentral gyrus. The mean extent of resection was 89.4%. Univariate analyses revealed that identification of the motor area correlated significantly with age and localization to the precentral gyrus. Multivariate analyses showed that older age (≥ 45 years), larger tumor volume (> 35.5 cm3), and localization to the precentral gyrus were significantly correlated with failure to identify the motor area (p = 0.0021, 0.0484, and 0.0015, respectively). Localization to the precentral gyrus showed the highest odds ratio (14.135) of all regressors.

CONCLUSIONS

Identification of the motor area can be difficult when a supratentorial glioma is localized to the precentral gyrus. The authors’ findings are important when performing awake craniotomy for glioma located within or close to the motor area or the pyramidal tract. A combination of transcortical motor evoked potential monitoring and awake craniotomy including subcortical motor mapping may be needed for removal of gliomas showing negative responses in the motor area to preserve the motor-related subcortical fibers.

ABBREVIATIONS EOR = extent of resection; MEP = motor evoked potential; MMT = manual muscle testing.

In Brief

Identification of the motor area during awake craniotomy is essential for preservation of motor function when resecting glioma within or close to the motor area or pyramidal tract. The authors believe that their study makes a significant contribution to the literature because its results show that identification of the motor area can be difficult when a supratentorial glioma is localized to the precentral gyrus.

Resection of gliomas located within or close to the motor area or pyramidal tract comes with a risk of severe motor dysfunction. Aggressive resection of intracranial glioma, which has a positive impact on the prognosis,1–6 may be associated with an increased risk of neurological complications. To avoid permanent postoperative motor dysfunction, identification of localization to the motor area is important. The most reliable method for identification of the eloquent motor areas is direct cortical brain mapping using electrical stimulation during awake craniotomy. Nevertheless, we sometimes encounter patients in whom the motor area cannot be identified with intraoperative functional mapping during awake craniotomy. Therefore, a knowledge of the factors related to difficulty in identification of the motor-related cortical area is essential when resecting gliomas located within or close to the motor area and pyramidal tract. However, these factors have not yet been elucidated.

Previously, we reported that identification of the frontal language area could be difficult on the dominant side in patients with frontal gliomas that involve the pars triangularis.7 It is well known that the pars triangularis plays an important role in the language network.8 Therefore, we speculated that neuroplasticity, which is a dynamic process,9,10 proceeds in stages and that scattered incomplete functional language reorganization occurs before neuroplasticity is completed on the dominant side in cases of frontal glioma involving the pars triangularis. Consequently, we hypothesized that this process makes identification of the frontal language area difficult. From these speculations, we suspected that a tumor location involving the essential functional cortical area is associated with a negative response to functional cortical mapping for supratentorial glioma during awake craniotomy.

More recently, we reported that combined evaluation of voluntary movement during awake craniotomy and transcortical motor evoked potentials (MEPs) was useful in 30 patients who underwent removal of glioma in the precentral gyrus.11 When analyzing the data in that study, we inferred empirically that the tumor localization was correlated with a negative response on motor cortical mapping and that identification of the motor area could be particularly difficult with gliomas localized in the precentral gyrus. The precentral gyrus is bordered anteriorly by the precentral sulcus, posteriorly by the postcentral gyrus, and caudally by the posterior ramus of the sylvian fissure. In the present study, we investigated 91 consecutive patients with primary supratentorial glioma located within or close to the motor area or pyramidal tract who underwent intraoperative cortical mapping to identify the motor area. The aim of the study was to determine whether or not tumor localization is correlated with a negative cortical response to motor mapping during awake craniotomy.

Methods

Patients and Preoperative Evaluation

Awake craniotomy was performed to preserve motor function in 137 patients with supratentorial glioma at Tokyo Women’s Medical University between April 2000 and May 2019. Ninety-one of these patients had primary glioma located within or close to the motor area or pyramidal tract and underwent intraoperative motor cortical mapping to identify the motor area. Of 137 patients, 46 with a recurrence were excluded from this study. In all patients the preoperative diagnosis was based on MRI studies, which included T1-weighted, T2-weighted, FLAIR, and postcontrast T1-weighted images. Using MR images, we evaluated whether or not the tumors localized to or involved the precentral gyrus. We defined a glioma as localizing to the precentral gyrus when more than 80% of the tumor was located in the precentral gyrus. We categorized preoperative motor dysfunction as “None” or “Declined.”

The study protocol was approved by the ethics committee of the Tokyo Women’s Medical University. The requirement for informed consent was waived in view of the retrospective design of the study. Patients were given the opportunity not to have their data included in the study via the opt-out method. To protect patient privacy, we removed all identifiers from our records on completion of our analyses.

Surgery

Surgery was performed according to the previously published concept of information-guided brain tumor removal, with the goal of maximal possible resection of the tumor with minimal risk of permanent postoperative neurological deficits.7,11–16 Intraoperative MRI (AIRIS II; Hitachi Medical Corp.) and an updated navigation system were used routinely. Surgery was generally performed with maximal possible removal of the totally enhanced area that was visualized on T1-weighted images for tumors suspected to be glioblastoma and on the hyperintense area on T2-weighted images for tumors suspected to be grade II or III glioma. Histopathological diagnosis of all tumors was based on the WHO criteria published in 2007.17

Continuous Monitoring of Transcortical MEPs and Functional Mapping During Awake Craniotomy

The following methods have been published previously.7,11,15,18 Briefly, to detect compound muscle action potentials, 27-gauge bipolar disposable subdermal needle electrodes were placed at a distance of approximately 10 mm apart on relevant muscles of the contralateral side of the tumor. Next, a 6-contact strip electrode was placed over the assumed rolandic region. Following positioning of the strip electrode, the median nerve was stimulated, and phase reversal of the somatosensory evoked potentials in the central sulcus and precentral gyrus was identified. The position of the strip electrode was adjusted to obtain the maximal compound muscle action potentials for the target muscles, with a threshold of 30 mA or less. Continuous MEP monitoring by direct cortical stimulation via the strip electrode (train stimulation 5 times; frequency 500 Hz; pulse duration 0.5 msec) was then performed with a neurophysiological monitoring device (Neuromaster MEE-1200; Nihon Kohden) during tumor removal. We defined a reduction in MEP amplitude of more than 50% as significant and reported this to the surgeon, as described previously.19–22

Using previously published methods for intraoperative brain mapping,7,11,15,18 electrical stimulation of the cortex was applied with repetitive square-wave biphasic currents of alternating polarity (pulse width 0.2 msec, frequency 50 Hz, duration 1–2 seconds) by using an Ojemann cortical stimulator (OCS-1; Integra Radionics, Inc.). A continuous digital electrocorticogram was monitored to detect seizures and afterdischarges. The stimulus intensity was increased steadily from 2 mA by using stepwise increments of 1 mA until an effect was attained or abnormalities on the electrocorticogram were noted. The maximum stimulus intensity was 6 mA (biphasic current; 12 mA). A positive motor response was confirmed by observing whether or not the relevant muscles moved. The MEP response was obtained by direct cortical stimulation, whereas negative motor response was confirmed by observing stimulation without the relevant muscle movement and the MEP response. To confirm that the results were reproducible, each cortical area was stimulated at least twice but never in succession. Removal of the tumor was accompanied by subcortical stimulation through the resection cavity and was intended to identify the motor pathways. The devices used for this purpose and the parameters of stimulation, including the intensity, were similar to those used for cortical mapping.23 During the entire procedure while the patient was awake, his or her voluntary movement was constantly monitored by observing the response to verbal commands from a member of the treatment team. When the team member confirmed that the patient’s voluntary movement had weakened, the degree of weakness was immediately reported to the surgeon. We categorized intraoperative voluntary movement as “No change” or “Declined” compared with the preoperative status.

Intraoperative and Postoperative Evaluation

The methods used have been published elsewhere.11,24 The tumor resection rate was assessed by intraoperative MRI. As previously reported,1,2,7,14,24 we used 3D Slicer 4.0 (freely downloadable from http://www.slicer.org ,25) for semiautomatic volumetry to evaluate the extent of resection (EOR). We calculated the EOR by using the contrast-enhanced area for enhanced tumors and the hyperintense areas on T2-weighted images for nonenhanced tumors intraoperatively. We evaluated the patient’s motor function on a daily basis until discharge from the hospital. Specifically, we categorized motor function 1 week after surgery as “Declined” or “No change” compared with the preoperative status. Thereafter, all patients were followed up regularly in the outpatient clinic by the attending neurosurgeon. We categorized motor function 6 months after surgery as “Declined” or “No change” compared with the preoperative status and further as “Mild,” “Moderate,” or “Severe,” as previously published.11,26 Motor function was assessed in all patients by manual muscle testing (MMT) as previously reported.11,27 Mild deficits included slight weakness and slight incoordination (MMT grade 4), which did not impact daily life. Moderate deficits included long-term weakness or a requirement for a brace when walking (MMT grade 2 or 3). Severe deficits included extreme motor weakness (MMT grade 0 or 1) and contracture.

Statistical Analyses

The data were analyzed using JMP Pro version 14.0 software (SAS Institute, Inc.). Associations between identification of the motor area and patient characteristics were assessed using Fisher’s exact test or the independent t-test. The cutoff value for age was selected by receiver operating characteristic curve analysis. Correlations between identification of the motor area and intraoperative/postoperative findings were evaluated by Fisher’s exact test or the independent t-test. Multivariate logistic regression analysis was used to explore the relationships between identification of the motor area and clinical characteristics, including localizing to the precentral gyrus. We analyzed age and tumor volume as both categorical and continuous variables, respectively, in multivariate logistic regression analysis. Statistical significance was defined as p < 0.05.

Results

Patient Demographics and Clinical Characteristics

The demographics of the patient population and their clinical characteristics are shown in Table 1. The mean age was 40.1 years (range 18–68 years). The mean tumor volume was 35.5 cm3 (SD 34.5 cm3). We classified tumor location as shown in Table 1. The mean EOR was 89.4%. The motor area could not be identified by electrical stimulation mapping during awake craniotomy in 16 (18%) of the 91 patients in the study. The motor areas could be identified in 75 patients (82%), and the motor areas were identified on the precentral gyrus in all 75 patients.

TABLE 1.

Summary of demographic and clinical characteristics of the study population

CharacteristicValue
No. of cases91
Sex
 Male58
 Female33
Mean age, yrs (range)40.1 (18–68)
Side of lesion
 Rt52
 Lt39
Mean tumor vol, cm335.5 ± 34.5
Tumor location
 SFG1
 MFG4
 IFG1
 SFG + MFG3
 MFG + IFG4
 SFG + MFG + IFG2
 PostCG7
 Insula2
 Cingulate gyrus2
 PreCG34
 SFG + PreCG8
 IFG + PreCG2
 SFG + MFG + PreCG3
 MFG + IFG + PreCG2
 PostCG + PreCG7
 SFG + PostCG + PreCG1
Mean EOR, %89.4 ± 14.0
WHO grade
 I2
 II42
 III35
 IV12
Identification of motor area
 Yes75
 No16

IFG = inferior frontal gyrus; MFG = middle frontal gyrus; PostCG = postcentral gyrus; PreCG = precentral gyrus; SFG = superior frontal gyrus.

Data are presented as number of patients or mean ± SD unless otherwise indicated.

Correlations Between Identification of the Motor Area and Patient Characteristics

The tumors were found to be localized to the precentral gyrus on MRI in 34 of the 91 patients and to involve the precentral gyrus in 58 patients (Table 2). The cutoff value for age from receiver operating characteristic curve analysis was 45 years. Therefore, we classified the 91 patients according to whether they were < 45 years or ≥ 45 years of age. Univariate analyses revealed that identification of the motor area correlated significantly with patient age and localization to the precentral gyrus (Table 2). Patient sex, whether the lesion was right-sided or left-sided, preoperative motor dysfunction, tumor volume, and involvement of the precentral gyrus were not associated with identification of the motor area.

TABLE 2.

Characteristics of patient subgroups according to whether or not the motor area was identified

Identification of Motor Area
CharacteristicYesNop Value*
No. of cases7516
Sex
 Male47110.6430
 Female285
Mean age, yrs39.1 ± 1.244.6 ± 3.00.0703
Age0.0072
 <45 yrs556
 ≥45 yrs2010
Side of lesion
 Rt4390.9367
 Lt327
Preop motor dysfunction0.6362
 None6214
 Declined132
Tumor vol, cm334.8 ± 3.638.7 ± 12.30.6892
Involvement of PreCG0.6430
 Yes4711
 No285
Localizing to PreCG
 Yes23110.0048
 No525

Data are presented as number of patients or mean ± SD.

Statistical analysis was performed by Fisher’s exact test or independent t-test.

The cutoff value for age (45 years) was detected by receiver operating characteristic analysis.

Correlations Between Identification of the Motor Area and Intraoperative/Postoperative Findings

Univariate analyses showed no significant correlation between identification of the motor area and any intraoperative/postoperative findings, including WHO grade (low or high grade), intraoperative transcortical MEP changes, and postoperative motor function (Table 3). In 9 of the 16 patients in whom the motor area could not be identified, motor-related subcortical fibers were detected by electrical stimulation.

TABLE 3.

Intraoperative and postoperative findings according to whether or not the motor area was identified

Identification of Motor Area
FindingYesNoUnivariate p Value*
No. of cases7516
EOR, %89.191.10.5967
WHO grade
 I200.4501
 II357
 III305
 IV84
WHO grade (low or high)0.7860
 Low grade (I, II)377
 High grade (III, IV)389
Identification of motor-related subcortical fibers0.3197
 Yes489
 No145
 NA132
Changes in transcortical MEP response0.5362
 MEP decline ≤50%223
 MEP decline >50%4812
 NA51
Voluntary movement intraop0.3960
 No change294
 Declined4612
Motor function 1 wk postop0.3778
 No change203
 Declined5513
Motor function 6 mos postop0.2535
 No change5412
 Declined (mild)163
 Declined (moderate)50
 Declined (severe)01

NA = not applicable.

Statistical analysis performed by Fisher’s exact test or independent t-test.

Multivariate Analysis of Potential Predictors of Identification of the Motor Area

Multivariate analyses with the logistic regression model showed that older age (≥ 45 years), a larger tumor volume (> 35.5 cm3), and localization to the precentral gyrus were significantly correlated with failure to identify the motor area (p = 0.0021, 0.0484, and 0.0015, respectively; Table 4). Localizing to the precentral gyrus showed the highest odds ratio (14.135; p = 0.0015) of all the regressors. When age and tumor volume were analyzed as continuous variables, older age, larger tumor volume, and localization to the precentral gyrus were also significantly correlated with failure to identify the motor area (p = 0.0129, 0.0162, and 0.0016, respectively; Table 4). Consequently, identification of the motor area was significantly difficult in patients with supratentorial glioma localizing to the precentral gyrus.

TABLE 4.

Logistic regression model predicting identification of the motor area

RegressorOR95% CIp Value*
Age (cutoff 45 yrs) (≥45 yrs vs <45 yrs)9.7102.286 to 41.2480.0021
Sex (female vs male)1.0150.239 to 4.3100.9840
Side of lesion (lt vs rt)2.0840.524 to 8.2790.2969
Tumor vol (mean 35.5 cm3) (>35.5 cm3 vs ≤35.5 cm3)5.3901.012 to 28.7150.0484
Localizing to PreCG (yes vs no)14.1352.763 to 72.3250.0015
AgeNA−0.156 to −0.0180.0129
Sex (female vs male)1.4970.370 to 6.0510.5713
Side of lesion (lt vs rt)2.1460.585 to 7.8730.2496
Tumor volNA−0.045 to −0.0050.0162
Localizing to PreCG (yes vs no)16.3932.900 to 92.6610.0016

Statistical analysis was performed using a logistic regression model test.

Analyzed as categorical variables.

Analyzed as continuous variables.

Clinical Characteristics of 16 Patients Without Identification of the Motor Area

The clinical characteristics of the 16 patients in whom the motor area was not identified are shown in detail in Table 5. The mean age was 45 years (range 24–68 years). Only 2 (13%) of the patients showed preoperative motor dysfunction. Eleven (69%) of the patients had tumors localizing to the precentral gyrus, and motor-related subcortical fibers were identified in 9 (56%). One week after surgery, motor function worsened in 13 patients (81%). Six months after surgery, only 1 (6%) had a persistent severe motor deficit. The mean EOR by volumetry was 91% ± 7.3% (mean ± SD).

TABLE 5.

Summary of clinical characteristics in 16 patients without identification of the motor area

Intraop & Postop Motor Function
Case No.Age (yrs)SexSide of LesionPreop Motor DysfunctionTumor LocationTumor Vol (cm3)Tumor HistologyIdentification of Subcortical FibersMEP Decline #>50%Intraop1 Wk Postop6 Mos PostopEOR (%)
143MRtNonePreCG8.4AAYesNoDeclinedDeclinedNo change100
252FLtNonePreCG19.0OYesYesDeclinedDeclinedMild75
349MRtNonePreCG9.0OYesYesDeclinedDeclinedSevere85
431FLtNonePreCG19.0ONoNoDeclinedDeclinedNo change95
553MRtNonePreCG10.1GBMNoNADeclinedDeclinedNo change95
651MRtDeclinedPreCG4.6AAYesNoDeclinedDeclinedMild80
731FLtNonePreCG35.8ONoNoDeclinedDeclinedNo change85
856MRtNonePreCG3.9DAYesNoDeclinedDeclinedNo change100
950MRtNonePreCG30.6OYesNoDeclinedNo changeNo change95
1068MRtDeclinedPreCG10.4GBMYesNoNo changeDeclinedNo change90
1147MLtNonePreCG39.7AANoNoNo changeDeclinedNo change85
1233MLtNoneSFG + MFG + IFG152.3AANANoNo changeNo changeNo change90
1326MLtNoneSFG + MFG46.2GBMYesNoDeclinedDeclinedNo change95
1452FRtNoneMFG + IFG40.5AONANoNo changeNo changeNo change95
1524FRtNoneMFG + IFG167.3GBMYesYesDeclinedDeclinedMild95
1647MLtNoneSFG21.8ONoNoDeclinedDeclinedNo change98

AA = anaplastic astrocytoma; AO = anaplastic oligodendroglioma; DA = diffuse astrocytoma; GBM = glioblastoma; O = oligodendroglioma.

Illustrative Cases

Case A

The tumor in this patient was located in the left superior frontal gyrus without involvement of the precentral gyrus (Fig. 1). The patient was a 23-year-old woman who presented with partial seizures. She had no other neurological deficit preoperatively. During an awake craniotomy, electrical stimulation identified the motor cortical area for the right hand and leg. We removed the tumor with guidance from electrical cortical and subcortical motor functional mapping. We could not confirm the motor response from the white matter. However, the patient showed weakness of the right hand and leg intraoperatively because of supplementary motor area syndrome. During the procedure, there was no decrease in transcortical MEP. The EOR was 95%. The pathological diagnosis was diffuse astrocytoma. Her motor function showed full recovery at 6 months after surgery.

FIG. 1.
FIG. 1.

Case A. A representative case without localization to or involvement of the precentral gyrus. Preoperative FLAIR MR images (A, axial; B, sagittal) revealed a tumor with hyperintense signal in the left superior frontal gyrus without involvement of the precentral gyrus. An intraoperative photograph (C) showing that electrical stimulation could identify the motor cortical area for the right leg and hand. An intraoperative photograph (D) showing the resection cavity after removal of the tumor. Motor cortical area for the leg (circled 1) and hand (circled 2 and 3), with yellow lines indicating the central sulcus (C and D). Postoperative FLAIR MR images (E, axial; F, sagittal) revealed that 95% of the tumor was removed. Figure is available in color online only.

Case B

The tumor in this patient was located in the right superior frontal gyrus with involvement of the precentral gyrus (Fig. 2). The patient was a 41-year-old woman who presented with frequent partial seizures. She had no other neurological deficit preoperatively. During an awake craniotomy, electrical stimulation identified the motor cortical area for the left hand. We removed the tumor with guidance from electrical cortical and subcortical motor functional mapping. We confirmed the motor response of the left leg and shoulder in the white matter. The patient showed weakness of the right hand and leg intraoperatively because of supplementary motor area syndrome. The transcortical MEP did not decrease during the procedure. The EOR was 95%. The pathological diagnosis was diffuse astrocytoma. Her motor function showed full recovery at 6 months after surgery.

FIG. 2.
FIG. 2.

Case B. A representative case without localization to but involvement of the precentral gyrus. Preoperative axial T2-weighted images (A and B) showing a tumor with hyperintense signal in the right superior frontal gyrus with involvement of the precentral gyrus. An intraoperative photograph (C) showing that electrical stimulation could identify the motor cortical area for the left hand. An intraoperative photograph (D) showing the resection cavity. Motor cortical area for the hand (circled 1), with yellow lines indicating the central sulcus (C and D). Postoperative axial T2-weighted images (E and F) showing that 95% of the tumor was removed. Figure is available in color online only.

Case C

The tumor in this patient had localized to the right precentral gyrus (Fig. 3). The patient was a 43-year-old man who presented with headache. He had no neurological deficit preoperatively. During an awake craniotomy, electrical stimulation did not identify any motor cortical area but induced convulsions in the precentral gyrus (Fig. 3C). We removed the tumor with guidance from electrical cortical and subcortical motor functional mapping. We could confirm the motor response of the left deltoid, wrist, and hand in the white matter. The patient showed weakness of the right hand intraoperatively. During the procedure, transcortical MEP in the left abductor pollicis brevis muscle decreased to 20% of the control value. The EOR was 100%. The pathological diagnosis was anaplastic astrocytoma. His motor function recovered 6 months after surgery.

FIG. 3.
FIG. 3.

Case C. A representative case with localization to the precentral gyrus. Preoperative FLAIR MR images (A, axial; B, coronal) revealed a tumor with hyperintense signal in the right precentral gyrus. An intraoperative photograph (C) showing that electrical stimulations could not identify any motor cortical area but induced convulsions in the precentral gyrus (circled 0). An intraoperative photograph (D) after removal of the tumor shows the resection cavity and sites where a subcortical motor response was elicited for the left deltoid muscle (circled 1), wrist (circled 2), and hand (circled 3), with yellow lines indicating the central sulcus (C and D). Postoperative FLAIR MR images (E, axial; F, coronal) revealed that 98% of the tumor was removed. Figure is available in color online only.

Discussion

Main Findings

The results of this study suggest that tumor location in the precentral gyrus is associated with a negative response in motor cortical mapping during awake craniotomy. The motor area could not be identified in 16 (18%) of 91 patients with supratentorial glioma within or close to the motor area or pyramidal tract. The motor areas could be identified in 75 patients (82%), and these areas were identified on the precentral gyrus in all 75 patients. A negative response for the motor area was observed in 23 (68%) of 34 patients with glioma localizing to the precentral gyrus; the motor area could not be identified in only 5 (9%) of 57 patients with glioma that did not localize to the precentral gyrus. Multivariate analyses showed that not only localizing to the precentral gyrus but also older age (≥ 45 years or continuous value) and larger tumor volume (> 35.5 cm3 or continuous value) were significantly correlated with failure to identify the motor area. However, a tumor localizing to the precentral gyrus was the most significant predictor of failure to identify the motor area (OR 14.135; p = 0.0015), even after adjusting for other clinical factors (age, sex, side of lesion, and tumor volume). Therefore, we consider that these findings should be borne in mind when performing awake craniotomy for supratentorial glioma located within or close to the motor area or pyramidal tract.

Mechanism for Difficulty in Identifying the Motor Area in Patients With Glioma Localizing to the Precentral Gyrus

It is unclear why the rate of detection of a motor cortical area during awake craniotomy depends on whether or not a tumor localizes to the precentral gyrus. In the present study, the motor area was identified in only 11 (32%) of 34 patients whose tumor localized to the precentral gyrus. Several reports have demonstrated that reorganization of the motor cortical area due to brain plasticity plays an important role in patients with glioma involving the primary motor cortex.28–31 Furthermore, brain functional reorganization is thought to be the reason infiltrative gliomas near or within eloquent motor areas do not induce detectable motor dysfunction preoperatively.10 A recent report demonstrated that functional reorganization of the motor cortex can occur in the presence of not only low-grade gliomas but also glioblastomas located in the region of the central sulcus.32 We previously reported that tumor location involving the pars triangularis is significantly correlated with a negative response in language cortical mapping; the pars triangularis plays an important role in the language network, leading to marked functional reorganization in the presence of this type of glioma.7 Consequently, we speculated that scattered incomplete functional relocalization occurs before brain plasticity is completed. The precentral gyrus is of course crucial for the motor functional network. Therefore, as mentioned in our previous paper,7 in the 11 patients with glioma localizing to the precentral gyrus, scattered incomplete motor functional relocalization may have occurred, such that we could not identify scattered localized motor functional areas with limited bipolar electrical stimulation.

Correlation Between Failure to Identify the Motor Area and Age or Tumor Volume

Multivariate analyses with the logistic regression model in this study revealed that older age (≥ 45 years) and larger tumor volume (> 35.5 cm3) were significantly correlated with failure to identify the motor area (Table 4). An earlier report evaluated whether functional reorganization of the motor cortex is associated with the increase in tumor size that occurs with increasing disease duration by using functional MRI studies in 16 patients with primary glioblastoma located at the region of the central sulcus.32 The results of that study demonstrated that the intensity of activation and the number of activated clusters of small tumors (< 40 cm3) were almost always higher as compared with the large tumors (≥ 40 cm3). These results were consistent with our finding that the motor area was more difficult to identify in patients with a larger tumor volume (> 35.5 cm3) than in those with a lower tumor volume (≤ 35.5 cm3). Furthermore, they inferred that the processes of functional reorganization depend on the patient’s age and the degree of disease dynamics, with those being most pronounced at a younger age and during a chronic process.32 Therefore, they suspected these factors to be responsible for the less radical change in the pattern of reorganization associated with larger tumors in their study. Moreover, older age may induce incomplete motor functional relocalization. These hypotheses may explain why a larger tumor volume and older age were correlated with failure to identify the motor area in our present study.

Surgical Strategy for Glioma Located Within or Close to the Motor Area or Pyramidal Tract Showing Negative Responses for the Motor Area

In the present study, the motor area could not be identified in 16 (18%) of 91 patients with supratentorial glioma within or close to the motor area or pyramidal tract (Table 5). Furthermore, 11 (69%) of these patients had tumors localizing to the precentral gyrus. As mentioned above, the motor functional areas may not have been identified because of limited bipolar electrical stimulation in these patients, and we believe that the motor area was not absent. Indeed, motor-related subcortical fibers could be identified in 9 (56%) of the 16 patients (Table 5). Recently, we reported that combined evaluation of voluntary movement during awake craniotomy and transcortical MEP was useful for tumor removal in 30 patients with glioma in the precentral gyrus.11 We removed the tumors in our 16 patients by using this strategy, with guidance from subcortical electrical stimulation to preserve the pyramidal tract. One week after surgery, motor function worsened in 13 (81%) of these patients. However, 6 months after surgery, only 1 (6%) of the 16 patients had a persistent severe motor deficit (Table 5). Most recently, Zelitzki et al. reported the results of a comparison of the clinical outcome in patients undergoing awake (n = 44) versus general anesthesia (n = 41) surgery for brain tumors located within or adjacent to the motor pathways.33 They also recommended awake craniotomy for tumors located in these areas, given that patient feedback and collaboration is only possible during awake craniotomy. Furthermore, the information provided from patients may add further safety measures to ensure the integrity of motor function. Therefore, we consider that the combination of continuous transcortical MEP monitoring with awake craniotomy including subcortical motor functional mapping is useful for removal of gliomas located within or close to the motor area or pyramidal tract in patients showing negative responses for the motor area to preserve the motor-related subcortical fibers.

Limitations of the Study

This study has some limitations. First, although preoperative functional MRI is useful for identifying the motor area,29,30,32,34 few patients could be included in the analysis. Therefore, we could not directly evaluate the correlation between the results of electrical cortical mapping and activated areas on functional MRI. Second, our study was retrospective and conducted at a single institution. Therefore, prospective multiinstitutional studies are needed in the future to validate our observations. Third, we could not stimulate cortical areas outside of a craniotomy or in the sulci. Therefore, care is required when interpreting the absence of a motor cortical area on electrical stimulation. Fourth, no clear reason for the absence of positive language sites in patients with tumors localizing to the precentral gyrus has been elucidated.

Conclusions

We have demonstrated that identification of the motor area can be difficult in patients with supratentorial glioma localizing to the precentral gyrus. The findings of this study should be kept in mind when performing awake craniotomy for supratentorial glioma located within or close to the motor area or pyramidal tract. Specifically, a combination of continuous transcortical MEP monitoring with awake craniotomy including subcortical motor functional mapping may be needed to preserve motor-related subcortical fibers when removing gliomas located within or close to the motor area or pyramidal tract if responses for the motor area are negative. Further prospective studies that include functional MRI are essential to fully elucidate the reorganization of motor function in patients with supratentorial glioma localizing to the precentral gyrus.

Acknowledgments

This study was supported by the Japan Society for the Promotion of Science (JSPS) KAKENHI Grant No. 18K09006. Special thanks are devoted to Dr. Takashi Komori, Ms. Soko Ikuta, Asuka Komori, and Mr. Takashi Sakayori for valuable help with clinical work and data analysis.

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Muragaki, Saito. Acquisition of data: Saito, Tamura, Tsuzuki. Analysis and interpretation of data: Muragaki, Saito, Tamura. Drafting the article: Saito. Critically revising the article: Muragaki, Saito, Kawamata. Reviewed submitted version of manuscript: Tamura, Maruyama, Nitta, Tsuzuki, Fukui, Kawamata. Statistical analysis: Saito. Administrative/technical/material support: Tamura, Maruyama, Nitta, Fukui. Study supervision: Muragaki, Kawamata.

References

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    Fujii Y , Muragaki Y , Maruyama T , Threshold of the extent of resection for WHO Grade III gliomas: retrospective volumetric analysis of 122 cases using intraoperative MRI . J Neurosurg . 2018 ;129 (1 ):1 9 .

    • Search Google Scholar
    • Export Citation
  • 2

    Fukui A , Muragaki Y , Saito T , Volumetric analysis using low-field intraoperative magnetic resonance imaging for 168 newly diagnosed supratentorial glioblastomas: effects of extent of resection and residual tumor volume on survival and recurrence . World Neurosurg . 2017 ;98 :73 80 .

    • Search Google Scholar
    • Export Citation
  • 3

    Lacroix M , Abi-Said D , Fourney DR , A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival . J Neurosurg . 2001 ;95 (2 ):190 198 .

    • Search Google Scholar
    • Export Citation
  • 4

    Nitta M , Muragaki Y , Maruyama T , Proposed therapeutic strategy for adult low-grade glioma based on aggressive tumor resection . Neurosurg Focus . 2015 ;38 (1 ):E7 .

    • Search Google Scholar
    • Export Citation
  • 5

    Sanai N , Polley MY , McDermott MW , An extent of resection threshold for newly diagnosed glioblastomas . J Neurosurg . 2011 ;115 (1 ):3 8 .

    • Search Google Scholar
    • Export Citation
  • 6

    Smith JS , Chang EF , Lamborn KR , Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas . J Clin Oncol . 2008 ;26 (8 ):1338 1345 .

    • Search Google Scholar
    • Export Citation
  • 7

    Saito T , Muragaki Y , Maruyama T , Difficulty in identification of the frontal language area in patients with dominant frontal gliomas that involve the pars triangularis . J Neurosurg . 2016 ;125 (4 ):803 811 .

    • Search Google Scholar
    • Export Citation
  • 8

    Sahin NT , Pinker S , Cash SS , Sequential processing of lexical, grammatical, and phonological information within Broca’s area . Science . 2009 ;326 (5951 ):445 449 .

    • Search Google Scholar
    • Export Citation
  • 9

    Duffau H . The huge plastic potential of adult brain and the role of connectomics: new insights provided by serial mappings in glioma surgery . Cortex . 2014 ;58 :325 337 .

    • Search Google Scholar
    • Export Citation
  • 10

    Duffau H . Lessons from brain mapping in surgery for low-grade glioma: insights into associations between tumour and brain plasticity . Lancet Neurol . 2005 ;4 (8 ):476 486 .

    • Search Google Scholar
    • Export Citation
  • 11

    Saito T , Muragaki Y , Tamura M , Awake craniotomy with transcortical motor evoked potential monitoring for resection of gliomas in the precentral gyrus: utility for predicting motor function . J Neurosurg . 2020 ;132 (4 ):987 997 .

    • Search Google Scholar
    • Export Citation
  • 12

    Muragaki Y , Iseki H , Maruyama T , Usefulness of intraoperative magnetic resonance imaging for glioma surgery . Acta Neurochir Suppl (Wien) . 2006 ;98 :67 75 .

    • Search Google Scholar
    • Export Citation
  • 13

    Muragaki Y , Iseki H , Maruyama T , Information-guided surgical management of gliomas using low-field-strength intraoperative MRI . Acta Neurochir Suppl (Wien) . 2011 ;109 :67 72 .

    • Search Google Scholar
    • Export Citation
  • 14

    Saito T , Muragaki Y , Maruyama T , Influence of wide opening of the lateral ventricle on survival for supratentorial glioblastoma patients with radiotherapy and concomitant temozolomide-based chemotherapy [published online November 8, 2019]. Neurosurg Rev. doi:10.1007/s10143-019-01185-2

    • Search Google Scholar
    • Export Citation
  • 15

    Saito T , Tamura M , Muragaki Y , Intraoperative cortico-cortical evoked potentials for the evaluation of language function during brain tumor resection: initial experience with 13 cases . J Neurosurg . 2014 ;121 (4 ):827 838 .

    • Search Google Scholar
    • Export Citation
  • 16

    Tamura M , Muragaki Y , Saito T , Strategy of surgical resection for glioma based on intraoperative functional mapping and monitoring . Neurol Med Chir (Tokyo) . 2015 ;55 (5 ):383 398 .

    • Search Google Scholar
    • Export Citation
  • 17

    Louis DN , Ohgaki H , Wiestler OD , The 2007 WHO classification of tumours of the central nervous system . Acta Neuropathol . 2007 ;114 (2 ):97 109 .

    • Search Google Scholar
    • Export Citation
  • 18

    Saito T , Muragaki Y , Tamura M , Impact of connectivity between the pars triangularis and orbitalis on identifying the frontal language area in patients with dominant frontal gliomas [published online November 10, 2018]. Neurosurg Rev. doi:10.1007/s10143-018-1052-z

    • Search Google Scholar
    • Export Citation
  • 19

    Krieg SM , Shiban E , Droese D , Predictive value and safety of intraoperative neurophysiological monitoring with motor evoked potentials in glioma surgery . Neurosurgery . 2012 ;70 (5 ):1060 1071 .

    • Search Google Scholar
    • Export Citation
  • 20

    Saito T , Muragaki Y , Maruyama T , Intraoperative functional mapping and monitoring during glioma surgery . Neurol Med Chir (Tokyo) . 2015 ;55 (suppl 1 ):1 13 .

    • Search Google Scholar
    • Export Citation
  • 21

    Saito T , Tamura M , Chernov MF , Neurophysiological monitoring and awake craniotomy for resection of intracranial gliomas . Prog Neurol Surg . 2018 ;30 :117 158 .

    • Search Google Scholar
    • Export Citation
  • 22

    Suess O , Suess S , Brock M , Kombos T . Intraoperative electrocortical stimulation of Brodman area 4: a 10-year analysis of 255 cases . Head Face Med . 2006 ;2 :20 .

    • Search Google Scholar
    • Export Citation
  • 23

    Kayama T . The guidelines for awake craniotomy guidelines committee of the Japan awake surgery conference . Neurol Med Chir (Tokyo) . 2012 ;52 (3 ):119 141 .

    • Search Google Scholar
    • Export Citation
  • 24

    Saito T , Muragaki Y , Shioyama T , Malignancy index using intraoperative flow cytometry is a valuable prognostic factor for glioblastoma treated with radiotherapy and concomitant temozolomide . Neurosurgery . 2019 ;84 (3 ):662 672 .

    • Search Google Scholar
    • Export Citation
  • 25

    Egger J , Kapur T , Fedorov A , GBM volumetry using the 3D Slicer medical image computing platform . Sci Rep . 2013 ;3 :1364 .

  • 26

    Magill ST , Han SJ , Li J , Berger MS . Resection of primary motor cortex tumors: feasibility and surgical outcomes . J Neurosurg . 2018 ;129 (4 ):961 972 .

    • Search Google Scholar
    • Export Citation
  • 27

    Takakura T , Muragaki Y , Tamura M , Navigated transcranial magnetic stimulation for glioma removal: prognostic value in motor function recovery from postsurgical neurological deficits . J Neurosurg . 2017 ;127 (4 ):877 891 .

    • Search Google Scholar
    • Export Citation
  • 28

    Duffau H . Contribution of cortical and subcortical electrostimulation in brain glioma surgery: methodological and functional considerations . Neurophysiol Clin . 2007 ;37 (6 ):373 382 .

    • Search Google Scholar
    • Export Citation
  • 29

    Fandino J , Kollias SS , Wieser HG , Intraoperative validation of functional magnetic resonance imaging and cortical reorganization patterns in patients with brain tumors involving the primary motor cortex . J Neurosurg . 1999 ;91 (2 ):238 250 .

    • Search Google Scholar
    • Export Citation
  • 30

    Niu C , Zhang M , Min Z , Motor network plasticity and low-frequency oscillations abnormalities in patients with brain gliomas: a functional MRI study . PLoS One . 2014 ;9 (5 ):e96850 .

    • Search Google Scholar
    • Export Citation
  • 31

    Takahashi S , Jussen D , Vajkoczy P , Picht T . Plastic relocation of motor cortex in a patient with LGG (low grade glioma) confirmed by NBS (navigated brain stimulation) . Acta Neurochir (Wien) . 2012 ;154 (11 ):2003 2008 .

    • Search Google Scholar
    • Export Citation
  • 32

    Majos A , Bryszewski B , Kośla KN , Process of the functional reorganization of the cortical centers for movement in GBM patients: fMRI study . Clin Neuroradiol . 2017 ;27 (1 ):71 79 .

    • Search Google Scholar
    • Export Citation
  • 33

    Zelitzki R , Korn A , Arial E , Comparison of motor outcome in patients undergoing awake vs general anesthesia surgery for brain tumors located within or adjacent to the motor pathways . Neurosurgery . 2019 ;85 (3 ):E470 E476 .

    • Search Google Scholar
    • Export Citation
  • 34

    Vassal M , Charroud C , Deverdun J , Recovery of functional connectivity of the sensorimotor network after surgery for diffuse low-grade gliomas involving the supplementary motor area . J Neurosurg . 2017 ;126 (4 ):1181 1190 .

    • Search Google Scholar
    • Export Citation

If the inline PDF is not rendering correctly, you can download the PDF file here.

Contributor Notes

Correspondence Yoshihiro Muragaki: Institute of Advanced Biomedical Engineering and Science, Tokyo Women’s Medical University, Tokyo, Japan. ymuragaki@twmu.ac.jp.

INCLUDE WHEN CITING Published online May 1, 2020; DOI: 10.3171/2020.2.JNS193471.

Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

  • View in gallery

    Case A. A representative case without localization to or involvement of the precentral gyrus. Preoperative FLAIR MR images (A, axial; B, sagittal) revealed a tumor with hyperintense signal in the left superior frontal gyrus without involvement of the precentral gyrus. An intraoperative photograph (C) showing that electrical stimulation could identify the motor cortical area for the right leg and hand. An intraoperative photograph (D) showing the resection cavity after removal of the tumor. Motor cortical area for the leg (circled 1) and hand (circled 2 and 3), with yellow lines indicating the central sulcus (C and D). Postoperative FLAIR MR images (E, axial; F, sagittal) revealed that 95% of the tumor was removed. Figure is available in color online only.

  • View in gallery

    Case B. A representative case without localization to but involvement of the precentral gyrus. Preoperative axial T2-weighted images (A and B) showing a tumor with hyperintense signal in the right superior frontal gyrus with involvement of the precentral gyrus. An intraoperative photograph (C) showing that electrical stimulation could identify the motor cortical area for the left hand. An intraoperative photograph (D) showing the resection cavity. Motor cortical area for the hand (circled 1), with yellow lines indicating the central sulcus (C and D). Postoperative axial T2-weighted images (E and F) showing that 95% of the tumor was removed. Figure is available in color online only.

  • View in gallery

    Case C. A representative case with localization to the precentral gyrus. Preoperative FLAIR MR images (A, axial; B, coronal) revealed a tumor with hyperintense signal in the right precentral gyrus. An intraoperative photograph (C) showing that electrical stimulations could not identify any motor cortical area but induced convulsions in the precentral gyrus (circled 0). An intraoperative photograph (D) after removal of the tumor shows the resection cavity and sites where a subcortical motor response was elicited for the left deltoid muscle (circled 1), wrist (circled 2), and hand (circled 3), with yellow lines indicating the central sulcus (C and D). Postoperative FLAIR MR images (E, axial; F, coronal) revealed that 98% of the tumor was removed. Figure is available in color online only.

  • 1

    Fujii Y , Muragaki Y , Maruyama T , Threshold of the extent of resection for WHO Grade III gliomas: retrospective volumetric analysis of 122 cases using intraoperative MRI . J Neurosurg . 2018 ;129 (1 ):1 9 .

    • Search Google Scholar
    • Export Citation
  • 2

    Fukui A , Muragaki Y , Saito T , Volumetric analysis using low-field intraoperative magnetic resonance imaging for 168 newly diagnosed supratentorial glioblastomas: effects of extent of resection and residual tumor volume on survival and recurrence . World Neurosurg . 2017 ;98 :73 80 .

    • Search Google Scholar
    • Export Citation
  • 3

    Lacroix M , Abi-Said D , Fourney DR , A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival . J Neurosurg . 2001 ;95 (2 ):190 198 .

    • Search Google Scholar
    • Export Citation
  • 4

    Nitta M , Muragaki Y , Maruyama T , Proposed therapeutic strategy for adult low-grade glioma based on aggressive tumor resection . Neurosurg Focus . 2015 ;38 (1 ):E7 .

    • Search Google Scholar
    • Export Citation
  • 5

    Sanai N , Polley MY , McDermott MW , An extent of resection threshold for newly diagnosed glioblastomas . J Neurosurg . 2011 ;115 (1 ):3 8 .

    • Search Google Scholar
    • Export Citation
  • 6

    Smith JS , Chang EF , Lamborn KR , Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas . J Clin Oncol . 2008 ;26 (8 ):1338 1345 .

    • Search Google Scholar
    • Export Citation
  • 7

    Saito T , Muragaki Y , Maruyama T , Difficulty in identification of the frontal language area in patients with dominant frontal gliomas that involve the pars triangularis . J Neurosurg . 2016 ;125 (4 ):803 811 .

    • Search Google Scholar
    • Export Citation
  • 8

    Sahin NT , Pinker S , Cash SS , Sequential processing of lexical, grammatical, and phonological information within Broca’s area . Science . 2009 ;326 (5951 ):445 449 .

    • Search Google Scholar
    • Export Citation
  • 9

    Duffau H . The huge plastic potential of adult brain and the role of connectomics: new insights provided by serial mappings in glioma surgery . Cortex . 2014 ;58 :325 337 .

    • Search Google Scholar
    • Export Citation
  • 10

    Duffau H . Lessons from brain mapping in surgery for low-grade glioma: insights into associations between tumour and brain plasticity . Lancet Neurol . 2005 ;4 (8 ):476 486 .

    • Search Google Scholar
    • Export Citation
  • 11

    Saito T , Muragaki Y , Tamura M , Awake craniotomy with transcortical motor evoked potential monitoring for resection of gliomas in the precentral gyrus: utility for predicting motor function . J Neurosurg . 2020 ;132 (4 ):987 997 .

    • Search Google Scholar
    • Export Citation
  • 12

    Muragaki Y , Iseki H , Maruyama T , Usefulness of intraoperative magnetic resonance imaging for glioma surgery . Acta Neurochir Suppl (Wien) . 2006 ;98 :67 75 .

    • Search Google Scholar
    • Export Citation
  • 13

    Muragaki Y , Iseki H , Maruyama T , Information-guided surgical management of gliomas using low-field-strength intraoperative MRI . Acta Neurochir Suppl (Wien) . 2011 ;109 :67 72 .

    • Search Google Scholar
    • Export Citation
  • 14

    Saito T , Muragaki Y , Maruyama T , Influence of wide opening of the lateral ventricle on survival for supratentorial glioblastoma patients with radiotherapy and concomitant temozolomide-based chemotherapy [published online November 8, 2019]. Neurosurg Rev. doi:10.1007/s10143-019-01185-2

    • Search Google Scholar
    • Export Citation
  • 15

    Saito T , Tamura M , Muragaki Y , Intraoperative cortico-cortical evoked potentials for the evaluation of language function during brain tumor resection: initial experience with 13 cases . J Neurosurg . 2014 ;121 (4 ):827 838 .

    • Search Google Scholar
    • Export Citation
  • 16

    Tamura M , Muragaki Y , Saito T , Strategy of surgical resection for glioma based on intraoperative functional mapping and monitoring . Neurol Med Chir (Tokyo) . 2015 ;55 (5 ):383 398 .

    • Search Google Scholar
    • Export Citation
  • 17

    Louis DN , Ohgaki H , Wiestler OD , The 2007 WHO classification of tumours of the central nervous system . Acta Neuropathol . 2007 ;114 (2 ):97 109 .

    • Search Google Scholar
    • Export Citation
  • 18

    Saito T , Muragaki Y , Tamura M , Impact of connectivity between the pars triangularis and orbitalis on identifying the frontal language area in patients with dominant frontal gliomas [published online November 10, 2018]. Neurosurg Rev. doi:10.1007/s10143-018-1052-z

    • Search Google Scholar
    • Export Citation
  • 19

    Krieg SM , Shiban E , Droese D , Predictive value and safety of intraoperative neurophysiological monitoring with motor evoked potentials in glioma surgery . Neurosurgery . 2012 ;70 (5 ):1060 1071 .

    • Search Google Scholar
    • Export Citation
  • 20

    Saito T , Muragaki Y , Maruyama T , Intraoperative functional mapping and monitoring during glioma surgery . Neurol Med Chir (Tokyo) . 2015 ;55 (suppl 1 ):1 13 .

    • Search Google Scholar
    • Export Citation
  • 21

    Saito T , Tamura M , Chernov MF , Neurophysiological monitoring and awake craniotomy for resection of intracranial gliomas . Prog Neurol Surg . 2018 ;30 :117 158 .

    • Search Google Scholar
    • Export Citation
  • 22

    Suess O , Suess S , Brock M , Kombos T . Intraoperative electrocortical stimulation of Brodman area 4: a 10-year analysis of 255 cases . Head Face Med . 2006 ;2 :20 .

    • Search Google Scholar
    • Export Citation
  • 23

    Kayama T . The guidelines for awake craniotomy guidelines committee of the Japan awake surgery conference . Neurol Med Chir (Tokyo) . 2012 ;52 (3 ):119 141 .

    • Search Google Scholar
    • Export Citation
  • 24

    Saito T , Muragaki Y , Shioyama T , Malignancy index using intraoperative flow cytometry is a valuable prognostic factor for glioblastoma treated with radiotherapy and concomitant temozolomide . Neurosurgery . 2019 ;84 (3 ):662 672 .

    • Search Google Scholar
    • Export Citation
  • 25

    Egger J , Kapur T , Fedorov A , GBM volumetry using the 3D Slicer medical image computing platform . Sci Rep . 2013 ;3 :1364 .

  • 26

    Magill ST , Han SJ , Li J , Berger MS . Resection of primary motor cortex tumors: feasibility and surgical outcomes . J Neurosurg . 2018 ;129 (4 ):961 972 .

    • Search Google Scholar
    • Export Citation
  • 27

    Takakura T , Muragaki Y , Tamura M , Navigated transcranial magnetic stimulation for glioma removal: prognostic value in motor function recovery from postsurgical neurological deficits . J Neurosurg . 2017 ;127 (4 ):877 891 .

    • Search Google Scholar
    • Export Citation
  • 28

    Duffau H . Contribution of cortical and subcortical electrostimulation in brain glioma surgery: methodological and functional considerations . Neurophysiol Clin . 2007 ;37 (6 ):373 382 .

    • Search Google Scholar
    • Export Citation
  • 29

    Fandino J , Kollias SS , Wieser HG , Intraoperative validation of functional magnetic resonance imaging and cortical reorganization patterns in patients with brain tumors involving the primary motor cortex . J Neurosurg . 1999 ;91 (2 ):238 250 .

    • Search Google Scholar
    • Export Citation
  • 30

    Niu C , Zhang M , Min Z , Motor network plasticity and low-frequency oscillations abnormalities in patients with brain gliomas: a functional MRI study . PLoS One . 2014 ;9 (5 ):e96850 .

    • Search Google Scholar
    • Export Citation
  • 31

    Takahashi S , Jussen D , Vajkoczy P , Picht T . Plastic relocation of motor cortex in a patient with LGG (low grade glioma) confirmed by NBS (navigated brain stimulation) . Acta Neurochir (Wien) . 2012 ;154 (11 ):2003 2008 .

    • Search Google Scholar
    • Export Citation
  • 32

    Majos A , Bryszewski B , Kośla KN , Process of the functional reorganization of the cortical centers for movement in GBM patients: fMRI study . Clin Neuroradiol . 2017 ;27 (1 ):71 79 .

    • Search Google Scholar
    • Export Citation
  • 33

    Zelitzki R , Korn A , Arial E , Comparison of motor outcome in patients undergoing awake vs general anesthesia surgery for brain tumors located within or adjacent to the motor pathways . Neurosurgery . 2019 ;85 (3 ):E470 E476 .

    • Search Google Scholar
    • Export Citation
  • 34

    Vassal M , Charroud C , Deverdun J , Recovery of functional connectivity of the sensorimotor network after surgery for diffuse low-grade gliomas involving the supplementary motor area . J Neurosurg . 2017 ;126 (4 ):1181 1190 .

    • Search Google Scholar
    • Export Citation

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