As preservation of neurocognitive function plays a crucial role in quality of life, it has become a primary goal in surgical approaches for glioma patients. Additionally, accurate assessment of neurocognitive function enhances intraoperative mapping and the safety of the procedure. Perioperative neurocognitive assessment is fundamental for evaluating the preservation of the functional margins and improving the learning curve of the entire team involved in patient management.
Neurocognitive deficits are common among individuals diagnosed with glioma, due to the adjuvant treatment and the slow growth of the tumor[17]. Most frequently, executive functions (higher-level cognitive processes responsible for planning, organizing and problem-solving) and memory are involved[18]. Hence, it is essential to diagnose previous cognitive deficits in order to correctly select patients to undergo awake craniotomy. The patient should hold skills for effective expression and communication, be able to perform the requested task and report any discomfort he may experience. Additionally, it is desirable that he maintains memory capabilities to retain instructions during surgery, and preserved visual abilities, particularly to perform tasks involving object naming and semantic[19]. Therefore, a straightforward preoperative neurophysiologic assessment is fundamental to evaluate these cognitive domains before awake surgery and track the results postoperatively.
The severity and type of neuropsychological impairment play a crucial role in determining the quality of life for individuals with glial tumors. Correct interpretation of intraoperative mapping relies on understanding the patient’s previous cognitive deficits. Acquiring precise information about a person's neuropsychological condition is essential for designing appropriate rehabilitation and supportive care plans[20, 21]. While not assessed in the current study, this protocol can be readily employed for ongoing patient follow-up during the treatment of glial neoplasia, allowing for the evaluation of phenomena such as chemobrain and the effects of radiotherapy. Neuropsychological functioning has been shown to have implications for prognosis and tumor recurrence, and it may even be more sensitive than imaging techniques in predicting early tumor recurrence[22, 23].
While choosing the neuropsychological assessment, an important practical consideration in both research and clinical settings is the trade-off between specificity and brevity[20, 24, 25]. Given that individuals with brain tumors often experience fatigue and psychological distress, administering a lengthy test battery not only burdens the individual but also risks compromising the validity of the test results[20]. Hence, it is crucial to strike a balance between specificity and brevity in neuropsychological testing to ensure the generation of valid and meaningful information[20]. The OMFTCT can be fully applied within a maximum of 35 minutes and has been routinely conducted at the patient's bedside, both one day before the surgical procedure and on the day of discharge from the hospital. Furthermore, qualitative analysis has shown consistent results across different testers. These attributes render the test highly adaptable and inclusive, facilitating preoperative cognitive assessments even in facilities lacking specialized neuropsychologists.
Naming ability plays a pivotal role in surgical protocols due to its association with various language areas distributed across different brain lobes and tracts. Consequently, OMFTCT incorporates naming tasks, while the BNT short version is exclusively focused on object naming. Therefore, OMFTCT was designed to encompass additional cognitive domains typically assessed in comprehensive neuropsychological evaluations. We've adapted these assessments to reduce administration time and minimize patient fatigue. Conducting a more extensive preoperative diagnosis enables safer and more comprehensive intraoperative testing. In our practice, we adhere to a rule that any function not assessed previously should not be included in the surgical mapping, as it could lead to false-positive mappings. Nevertheless, functions that go untested are susceptible to potential damage during tumor resection.
OMFTCT demonstrated a moderate correlation (r = 0.6) with statistical significance (p = 0.02) when compared to the gold standard BNT short version, aligning with deficits identified by low scores on the BNT short version. Furthermore, OMFTCT effectively identified visual deficits. The inclusion of various cognitive tasks in the primary assessment allows the detection of impairments that the patient, as well as their closest relatives and friends, may not be aware of. Due to the slow growth of tumors and neuroplasticity, subtle changes in cognitive abilities can go unnoticed. Identifying these changes is imperative for planning an appropriate intraoperative protocol.
The optimization of the intraoperative language protocol is crucial because awake testing typically lasts 1.5 to 2 hours, during which the patient may become distressed and fatigued. Therefore, the protocol should prioritize testing the most likely functions in the vicinity of the manipulated brain area. The choice of tests is determined by the surgeon's orientation and requirements, as well as clinical presentation, OMFTCT scores, and anatomical planning. However, there is a lack of literature data suggesting the optimal score that would ensure safe intraoperative testing. Mitchel Berger has suggested that a 25% error rate is acceptable for safe intraoperative testing[26, 27]. In our practice, we typically aim for scores in the range of 3 to 5.
In developing the protocol, our primary concern was to incorporate tests that had already been applied and validated in comprehensive neuropsychological assessment processes. However, we aimed to adapt these tasks to reduce the application time. Our goal was to prioritize an appropriate assessment duration that would minimize patient fatigue while still covering multiple cognitive domains. We also sought to include a sensitive measure, as suggested by Giovagnoli[28], to evaluate the overall cognitive abilities of these patients. Then, we proposed a practical and comprehensive test that can be easily administered within an average time of 23 minutes.
Among the cognitive symptoms observed in the preoperative period, memory deficit was the most common, affecting 38.9% of the sample. In terms of emotional complaints, the majority of patients (88.9%) did not exhibit mood alterations, except for 11.2%, who experienced irritability and anxiety. It is worth noting that these emotional symptoms were primarily attributed to the surgical context rather than being a direct result of the disease itself.
In general, glioma patients undergoing treatment are likely to experience medium to long-term deficits in memory and attention domains. The OMFTCT protocol correlates with BNT but also identifies visual memory deficits that are not assessed in the last one. The main findings indicate that visual memory impairment is the most prominent cognitive domain affected. Among the 36 evaluated patients, 20 exhibited visual memory deficits, with most of these lesions located in the left hemisphere.
A slight decline in performance was observed during the second evaluation period (48 hours after surgery) due to intraoperative manipulation, we further recovery. After a 30-day post-surgery period, the patients underwent the third application of the protocol. This timeframe is justified by the average duration in which patients are typically referred for adjuvant treatment, allowing the team to assess the patient's overall condition, including the emotional-cognitive component, before radiotherapy and/or chemotherapy.
Out of the 50 patients who completed the OMFTCT protocol, 14 were excluded from the study due to failure to complete the final stage of the evaluation. It is worth noting potential biases associated with this issue. We believe that patients who perform better in assessments and cognitive rehabilitation tend to have a better prognosis, which may lead to reduced therapeutic adherence. Therefore, it is crucial to emphasize the importance of completing all stages of the evaluation protocol to ensure a more comprehensive and individualized therapeutic strategy for these patients. Despite of being excluded, we correlated the T1 score with tumor location (Fig. 4).
The OMFTCT protocol offers a significant clinical advantage, as it does not necessitate the presence of a specialized neuropsychologist. It is easy and can be administered at the patient's bedside. However, it remains essential to have a neuropsychologist with expertise in cognitive assessment within the team. Their role includes the qualitative analysis of results, supervision of test administration to ensure consistency and standardization, and team training.Furthermore, the neuropsychologist can assess and address any emotional issues related to the illness, establishing a strong rapport with the patient that enhances adherence to cognitive rehabilitation. Another protocol advantage is its intraoperative replicability across all subtests.
One limitation of the study was the small sample size. However, the primary objective was to demonstrate the feasibility of a new fast-track protocol. Future studies with larger, more diverse populations, including patients with lower levels of education, may yield more comprehensive data.
In conclusion, the OMFTCT provided preoperative and postoperative assessments of various cognitive domains, enabling the effective planning of intraoperative cognitive testing. Moreover, immediate diagnosis of neurocognitive deficits played a crucial role in guiding patient care and rehabilitiation. The OMFTCT protocol demonstrated its representativeness and statistical significance when compared to the widely used BNT test for assessing similar patient populations.