Original ArticleFunctional-Based Resection Does Not Worsen Quality of Life in Patients with a Diffuse Low-Grade Glioma Involving Eloquent Brain Regions: A Prospective Cohort Study
Introduction
World Health Organization (WHO) diffusely infiltrative isocitrate dehydrogenase (IDH)-mutant grade II gliomas (diffuse low-grade gliomas [DLGGs])1 affect young adults with an active family, professional, social, and occupational life.2 DLGGs systematically progress3, 4 and induce epileptic seizures, neurologic deficits, and cognitive deficits, all impairing health-related quality of life and ability to work. Maximal safe surgical resection is the first therapeutic option, aiming at increasing survival and preserving, or even improving, health-related quality of life.5, 6, 7, 8, 9, 10, 11, 12
DLGGs located within eloquent regions pose a particular surgical challenge because of the higher risk of postoperative neurologic and cognitive deficits. This is an important issue because glioma survival, regardless of malignancy grade, is linked to the extent of resection and to the functional status of the patient.13, 14, 15, 16, 17 However, few studies have detailed the impact of a functional-based resection of a DLGG involving eloquent regions on postoperative health-related quality of life.18, 19, 20, 21 Although gross total resection is associated with improved health-related quality of life for patients with high-grade gliomas22 and with symptom resolution for patients with infiltrative gliomas,23 no data are available about the relationship between the extent of functional-based resection, the residual tumor, and health-related quality of life in patients with a DLGG involving eloquent areas.
We assessed prospectively the postoperative cognitive function and ability to work as a surrogate of health-related quality of life in a series of adult patients with a DLGG involving eloquent areas and having a functional-based maximal surgical resection according to functional boundaries using intraoperative corticosubcortical mapping under awake conditions. Based on previous literature, we hypothesized that: 1) functional-based surgical resection does not worsen postoperative cognitive and neurologic evaluations of patients with a DLGG involving eloquent regions; 2) large functional-based surgical resection improves postoperative cognitive and neurologic evaluations of patients with a DLGG involving eloquent regions; and 3) large functional-based surgical resection improves postoperative ability to work of patients with a DLGG involving eloquent regions.
Section snippets
Data Source
This prospective longitudinal study was conducted at a tertiary referral neurosurgical center between March 2010 and March 2016 for patients with brain tumor. The local human research institutional review board approved the study protocol (protocol number A01933-48). Patients were included at the time of initial diagnosis after neurosurgical intervention. An informed written consent was obtained from all patients prior to enrollment.
The following inclusion criteria were applied: 1) age ≥18
Study Population
Thirty-nine patients (18 males, 46.2%) undergoing a functional-based surgical resection without adjuvant oncologic treatment for a DLGG involving eloquent brain regions were prospectively included. All patients were fully cooperative; none of the experienced intraoperative seizures or required termination of the procedure. Illustrative cases are presented in Figure 1. No patient was lost to follow-up. The main characteristics of the population are detailed in Table 1.
Preoperative Functional Assessment
Thirty-two patients
Key Results
In this prospective cohort study including 39 adult patients, postoperative cognitive functioning improvement and postoperative ability to work, similar or superior to preoperative work capacity, significantly varied with extent of resection and with residual tumor. Maximal functional-based surgical resection for DLGGs involving eloquent brain regions is safe and correlates with improved cognitive outcomes and return to work rates.
Interpretation
The optimization of the oncofunctional balance is a concern in
Conclusions
As a practical consequence, a large functional-based resection using direct corticosubcortical electric stimulation under awake conditions to define functional boundaries is feasible with low morbidity in adult patients with a DLGG involving eloquent brain regions and helps the improvement of postoperative seizure control, cognitive function, and return to work, in addition to improving survival.
References (42)
Diffuse low-grade gliomas and neuroplasticity
Diagn Interv Imaging
(2014)- et al.
Operative techniques for gliomas and the value of extent of resection
Neurotherapeutics
(2009) - et al.
Functional and oncological outcomes following awake surgical resection using intraoperative cortico-subcortical functional mapping for supratentorial gliomas located in eloquent areas
Neurochirurgie
(2017) - et al.
Symptom resolution in infiltrating WHO grade II-IV glioma patients undergoing surgical resection
J Clin Neurosci
(2016) - et al.
Peri- and intraoperative cognitive and language assessment for surgical resection in brain eloquent structures
Neurochirurgie
(2017) - et al.
Direct electrical bipolar electrostimulation for functional cortical and subcortical cerebral mapping in awake craniotomy. Practical considerations
Neurochirurgie
(2017) - et al.
Response assessment in neuro-oncology (a report of the RANO group): assessment of outcome in trials of diffuse low-grade gliomas
Lancet Oncol
(2011) - et al.
Surgical strategies in low-grade gliomas and implications for long-term quality of life
J Clin Neurosci
(2014) - et al.
Cognitive and radiological effects of radiotherapy in patients with low-grade glioma: long-term follow-up
Lancet Neurol
(2009) - et al.
The 2016 World Health Organization Classification of Tumors of the Central Nervous System: a summary
Acta Neuropathol
(2016)
Prognostic value of initial magnetic resonance imaging growth rates for World Health Organization grade II gliomas
Ann Neurol
Velocity of tumor spontaneous expansion predicts long-term outcomes for diffuse low-grade gliomas
Neuro Oncol
Guidelines on management of low-grade gliomas: report of an EFNS-EANO Task Force
Eur J Neurol
Spontaneous and therapeutic prognostic factors in adult hemispheric World Health Organization Grade II gliomas: a series of 1097 cases: clinical article
J Neurosurg
Epileptic seizures in diffuse low-grade gliomas in adults
Brain
Comparison of a strategy favoring early surgical resection vs a strategy favoring watchful waiting in low-grade gliomas
JAMA
Extent of surgical resection is independently associated with survival in patients with hemispheric infiltrating low-grade gliomas
Neurosurgery
Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas
J Clin Oncol
Low-grade gliomas in adults
J Neurosurg
Glioma extent of resection and its impact on patient outcome
Neurosurgery
Impact of intraoperative stimulation brain mapping on glioma surgery outcome: a meta-analysis
J Clin Oncol
Cited by (31)
Adjuvant therapy and molecular profiling for inoperable gliomas
2019, New Techniques for Management of 'Inoperable' GliomasAnalysis of Legal, Cultural, and Socioeconomic Parameters in Low-Grade Glioma Management: Variability Across Countries and Implications for Awake Surgery
2018, World NeurosurgeryCitation Excerpt :This payment model is not suitable for rehabilitation therapy, because the specific program, duration, and frequency of therapy should be decided by the individual characteristics of each patient. Although working is important to QoL,32 it might be adapted to stop work temporarily in the immediate postoperative period to allow the patient to be engaged entirely with rehabilitation for a few weeks, ideally at home, in a familiar environment. Professional activity is a good rehabilitation activity per se; however, the optimal situation would be a progressive return to work (e.g., part-time initially).76
Verbal fluency predicts work resumption after awake surgery in low-grade glioma patients
2024, Acta NeurochirurgicaPreoperative assessment of eloquence in neurosurgery: a systematic review
2023, Journal of Neuro-Oncology
Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.