Alterations in Functional Connectomics Associated With Neurocognitive Changes Following Glioma Resection

Neurosurgery 88,(3)2021: 544–551

Decline in neurocognitive functioning (NCF) often occurs following brain tumor resection. Functional connectomics have shown how neurologic insults disrupt cerebral networks underlying NCF, though studies involving patients with brain tumors are lacking.

OBJECTIVE: To investigate the impact of brain tumor resection upon the connectome and relationships with NCF outcome in the early postoperative period.

METHODS: A total of 15 right-handed adults with left perisylvian glioma underwent resting-state functional magnetic resonance imaging (rs-fMRI) and neuropsychological assessment before and after awake tumor resection. Graph theoretical analysiswas applied to rs-fMRI connectivity matrices to calculate network properties. Network properties and NCF measures were compared across the pre- to postoperative periods with matched pairs Wilcoxon signed-rank tests.Associations between pre- to postoperative change in network and NCF measures were determined with Spearman rank-order correlations (ρ).

RESULTS: A majority of the sample showed postoperative decline on 1 or more NCF measures. Significant postoperative NCF decline was found across measures of verbal memory, processing speed, executive functioning, receptive language, and a composite index. Regarding connectomic properties, betweenness centrality and assortativity were significantly smaller postoperatively, and reductions in these measures were associated with better NCF outcomes. Significant inverse associations (ρ = −.51 to −.78, all P < .05) were observed between change in language, executive functioning, and learning and memory, and alterations in segregation, centrality, and resilience network properties.

CONCLUSION: Decline in NCF was common shortly following resection of glioma involving eloquent brain regions, most frequently in verbal learning/memory and executive functioning. Better postoperative outcomes accompanied reductions in centrality and resilience connectomic measures.

Supratotal Resection of Diffuse Frontal Lower Grade Gliomas with Awake Brain Mapping, Preserving Motor, Language, and Neurocognitive Functions

World Neurosurg. (2018) 119:30-39

Extended margin tumor resection beyond the abnormal area detected by magnetic resonance imaging, defined as supratotal resection, could improve the outcomes of patients with lower grade gliomas (LGGs). The aim of the present study was to assess the surgical outcomes of awake brain mapping to achieve supratotal resection with determination of the normal brain tissue boundaries beyond the tumor of frontal LGGs, in both dominant and nondominant hemispheres.

METHODS: We analyzed the data from 9 patients with diffuse frontal LGGs who had undergone supratotal resection with awake surgery from January 2016 to November 2017.

RESULTS: The frontal aslant tract was identified as the functional boundary in 4 of 5 left frontal tumor cases (80%). Working memory impairments during dorsolateral prefrontal cortex stimulation with digit span and/or visual N-back tasks were detected in all 4 patients (100%) with right-frontal tumor. The neurocognitive outcomes were significantly improved after surgery, as shown by the mean Wechsler adult intelligence scale III scores for verbal intelligence quotient (P [ 0.04) and verbal comprehension (P [ 0.03) and the mean Wechsler memory scale-revised scores for generalized memory (P [ 0.04) and delayed recall (P [ 0.04).

CONCLUSIONS: The results of the present study have provided evidence that awake mapping can enable the preservation of higher neurocognitive function, including working memory and spatial cognition in patients with nondominant right frontal tumors. Despite the small number of cases, our findings suggest the surgical benefit of awake surgery for supratotal resection of diffuse frontal LGGs.

Supratotal Resection of Diffuse Frontal Lower Grade Gliomas with Awake Brain Mapping, Preserving Motor, Language, and Neurocognitive Functions

World Neurosurg. (2018) 119:3039

Extended margin tumor resection beyond the abnormal area detected by magnetic resonance imaging, defined as supratotal resection, could improve the out- comes of patients with lower grade gliomas (LGGs). The aim of the present study was to assess the surgical outcomes of awake brain mapping to achieve supratotal resection with determination of the normal brain tissue boundaries beyond the tumor of frontal LGGs, in both dominant and nondominant hemispheres.

METHODS: We analyzed the data from 9 patients with diffuse frontal LGGs who had undergone supratotal resection with awake surgery from January 2016 to November 2017.

RESULTS: The frontal aslant tract was identified as the functional boundary in 4 of 5 left frontal tumor cases (80%). Working memory impairments during dorsolateral prefrontal cortex stimulation with digit span and/or visual N-back tasks were detected in all 4 patients (100%) with right-frontal tumor. The neurocognitive outcomes were significantly improved after surgery, as shown by the mean Wechsler adult intelligence scale III scores for verbal in- telligence quotient (P [ 0.04) and verbal comprehension (P [ 0.03) and the mean Wechsler memory scale-revised scores for generalized memory (P [ 0.04) and delayed recall (P [ 0.04).

CONCLUSIONS: The results of the present study have provided evidence that awake mapping can enable the preservation of higher neurocognitive function, including working memory and spatial cognition in patients with nondominant right frontal tumors. Despite the small number of cases, our findings suggest the surgical benefit of awake surgery for supratotal resection of diffuse frontal LGGs.

Cognitive functioning early after surgery of gliomas in eloquent areas

J Neurosurg 117:831–838, 2012

Patients with gliomas frequently have cognitive deficits, and surgery can exacerbate these deficits. Preoperative assessment is therefore crucial in patients undergoing surgery for glioma in eloquent areas, because the proximity of functional areas increases the risk of permanent postoperative cognitive disturbances. Although pre- and postoperative language and motor function in patients with glioma have been investigated frequently, data on good cognition studies are scarce. Most studies have focused on clinical neurological functioning or have only used brief neurological instruments. The authors investigated whether surgery for glioma in eloquent areas influences cognition early after surgery, by using an elaborate test protocol.

Methods. Twenty-eight patients with gliomas of the left hemisphere in language and nonlanguage areas were assessed before and 3 months after surgery with a comprehensive neuropsychological test protocol. The authors performed a correlation analysis between change in cognitive performance and tumor characteristics (that is, location, volume, pathological features, and histological grade) and between cognitive change and treatment-related factors (the extent of the resection and postoperative treatment with chemo- and radiotherapy).

Results. Both pre- and postoperatively, the mean performance of the patients was worse than the performance of the normal population in the language domain, the memory domain, and the executive functions (p < 0.05). Postoperatively, a decline was found in the language domain (t = 2.34, p = 0.027) and in the executive functions (t = 2.45, p = 0.022). However, cognitive change postsurgery was influenced by the location of the tumor; the decrease of cognitive score in the language domain was only observed in patients with tumors in or close to language areas (t = 2.33, p = 0.029). No effect on cognitive change was found for the other tumor characteristics and treatment-related factors.

Conclusions. This study underlines the importance of the use of a neuropsychological test protocol before and after surgery in patients with glioma, because several tasks in the domains of language, memory, and executive functions appeared to deteriorate after surgery. Tumor resection in language areas increases the risk of cognitive deficits in the language domain postoperatively.

Neurocognitive function before and after surgery for insular gliomas

J Neurosurg 115:1115–1125, 2011. DOI: 10.3171/2011.8.JNS11488

Insular gliomas can be resected with acceptable rates of neurological morbidity, but little is known with regard to impairment of higher-order neurocognitive functions. The frequency and functional impact of neurocognitive deficits in patients with gliomas has until recently been underappreciated. The authors therefore examined neurocognitive function in patients with insular gliomas and compared the findings in this group to those in a matched control group of patients with gliomas in nearby brain regions.

Methods. Thirty-three patients with WHO Grade II or III insular gliomas participated in neuropsychological evaluations before and after resection. To establish whether the pattern of neurocognitive performance was different from that of other patients with tumors in neighboring areas, patients with insular tumors were matched with control patients for age, educational level, preoperative Karnofsky Performance Scale score, tumor side, grade, and volume. The control group comprised patients in whom gliomas had been resected from frontal, temporal, and parietal areas near the insula. Baseline pre- and postoperative neurocognitive test results were compared between and within groups.

Results. Preoperative neurocognitive impairment was common in both insular and control groups. Patients with insular tumors had significantly worse preoperative performance on naming tests. In both groups, postoperative decline occurred in most neurocognitive domains. There were no statistically significant differences between patients in the insular and control groups with regard to rates of postoperative decline on any test. However, there were trends suggesting differential cognitive performance postoperatively, because patients with insular tumors were more likely to experience greater decline in learning and memory. Neurological morbidity was similar to prior rates reported in the literature.

Conclusions. Few statistically significant differences in cognitive function were observed between patients in the insular and control groups at either the pre- or postoperative evaluation, although there was a trend for patients with insular tumors to exhibit greater postoperative decline in learning and memory. Although technically more challenging, surgery for insular region glioma appears feasible without profound neurological or cognitive morbidity for many patients.