Neurocognitive and functional outcomes in patients with diffuse frontal lower-grade gliomas undergoing intraoperative awake brain mapping

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OBJECTIVE

Lower-grade gliomas (LGGs) are often observed within eloquent regions, which indicates that tumor resection in these areas carries a potential risk for neurological disturbances, such as motor deficit, language disorder, and/or neurocognitive impairments. Some patients with frontal tumors exhibit severe impairments of neurocognitive function, including working memory and spatial awareness, after tumor removal. The aim of this study was to investigate neurocognitive and functional outcomes of frontal LGGs in both the dominant and nondominant hemispheres after awake brain mapping.

METHODS

Data from 50 consecutive patients with diffuse frontal LGGs in the dominant and nondominant hemispheres who underwent awake brain surgery between December 2012 and September 2018 were retrospectively analyzed. The goal was to map neurocognitive functions such as working memory by using working memory tasks, including digit span testing and N-back tasks.

RESULTS

Due to awake language mapping, the frontal aslant tract was frequently identified as a functional boundary in patients with left superior frontal gyrus tumors (76.5%). Furthermore, functional boundaries were identified while evaluating verbal and spatial working memory function by stimulating the dorsolateral prefrontal cortex using the digit span and visual N-back tasks in patients with right superior frontal gyrus tumors (7.1%). Comparing the preoperative and postoperative neuropsychological assessments from the Wechsler Adult Intelligence Scale–Third Edition (WAIS-III) and Wechsler Memory Scale–Revised (WMS-R), significant improvement following awake surgery was observed in mean Perceptual Organization (Z = −2.09, p = 0.04) in WAIS-III scores. Postoperative mean WMS-R scores for Visual Memory (Z = −2.12, p = 0.03) and Delayed Recall (Z = −1.98, p = 0.04) were significantly improved compared with preoperative values for every test after awake surgery. No significant deterioration was noted with regard to neurocognitive functions in a comprehensive neuropsychological test battery. In the postoperative course, early transient speech and motor disturbances were observed in 30.0% and 28.0% of patients, respectively. In contrast, late permanent speech and motor disturbances were observed in 0% and 4.0%, respectively.

CONCLUSIONS

It is noteworthy that no significant postoperative deterioration was identified compared with preoperative status in a comprehensive neuropsychological assessment. The results demonstrated that awake functional mapping enabled favorable neurocognitive and functional outcomes after surgery in patients with diffuse frontal LGGs.

ABBREVIATIONS A/C = Attention/Concentration; CG = cingulate gyrus; DLPFC = dorsolateral prefrontal cortex; DR = Delayed Recall; EOR = extent of resection; FAT = frontal aslant tract; FIQ = Full IQ; GM = Generalized Memory; IFG = inferior frontal gyrus; LGG = lower-grade glioma; MFG = middle frontal gyrus; PG = precentral gyrus; PIQ = Performance IQ; PO = Perceptual Organization; PS = Processing Speed; SFG = superior frontal gyrus; SMA = supplementary motor area; VC = Verbal Comprehension; VeM = Verbal Memory; ViM = Visual Memory; VIQ = Verbal IQ; WAIS-III = Wechsler Adult Intelligence Scale–Third Edition; WM = Working Memory; WMS-R = Wechsler Memory Scale–Revised.

Article Information

Correspondence Kazuya Motomura: Nagoya University School of Medicine, Nagoya, Japan. kmotomura@med.nagoya-u.ac.jp.

INCLUDE WHEN CITING Published online May 17, 2019; DOI: 10.3171/2019.3.JNS19211.

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

© AANS, except where prohibited by US copyright law.

Headings

Figures

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    Case 48. A: Preoperative sagittal T2-weighted MR image revealing a left frontal LGG (left SFG) in a 36-year-old right-handed man with no relevant medical history. He presented with convulsive attacks and was transferred to a nearby hospital in June 2018. He was referred to our hospital to undergo tumor removal performed using awake surgery. B: Awake surgery was performed with cortical and subcortical mapping to identify the FAT and safely resect the tumor with FAT as the functional boundary. Intraoperative photograph obtained after the resection reveals letter tags that indicate the tumor boundaries (A–E). PG stimulation induced speech arrest (number tags: 1, 2, 3). FAT stimulation elicited delay in speech initiation and speech arrest (number tags: 22, 23, 26, 27, 28). Cortical mapping revealed the DLPFC on the lateral tumor side (number tag: 9), using a 4-digit backward digit span task and 2-back test to confirm verbal working memory. These positive mappings determined the limits of the tumor resection. The tumor was resected up to the interhemispheric fissure medially and the corpus callosum inferiorly. Consequently, the tumor was almost completely resected up to the functional boundaries. Yellow arrowheads designate the FAT; the white arrow points to the sylvian fissure. C: Postoperative sagittal FLAIR-weighted MR image revealing subtotal mass resection attained using awake brain mapping. The patient exhibited no postoperative impairments of neurocognitive status, language function, or motor paralysis. Figure is available in color online only.

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