Mesial temporal lobe epilepsy (MTLE) remains the most common and devastating form of epilepsy in clinical practice and is characterized by irreversible biochemical and structural alterations in the hypothalamus and several neocortical regions.[2-4] The estimated incidence of MTLE is 3.1 to 3.4 cases per 100,000 people per year in the United States. MTLE can be detrimental to quality of life because of recurrent seizures. Its effect on cognitive function remains controversial.
Although limited evidence suggests that patients with MTLE perform better in complex reaction time testing, a recent study has demonstrated that MTLE can contribute to problems with social cognition and emotion control. Patients with MTLE are more likely to suffer from depression and anxiety than normal people. These mood disturbances are associated with hippocampus sclerosis as visualized on magnetic resonance imaging (MRI).[10,11] Temporal lobe epilepsy (TLE) is often refractory to medical treatment but amenable to surgical treatment. The American Academy of Neurology recommends surgery as the treatment choice for medically intractable cases, mainly based on evidence from a single-center randomized clinical trial that demonstrated its efficacy in patients with longstanding TLE.[12,13]
Recent clinical evidence suggests that patients who received early surgical referral with continuing pharmaco-therapy post-operatively can achieve seizure freedom during the second post-operative year. Adolescents can also benefit from early surgery. In a cohort study that enrolled 1346 patients, Jehi et al reported that 67.9% of patients who underwent anterior temporal lobectomy achieved seizure freedom. Surgical treatment of patients with refractory seizures can result in improved cognition, behavior, and quality of life. However, removal of epileptic lesions may also trigger functional impairment of cognition, particularly on working memory and nomenclature. Some studies have argued that selective surgery preserves cognitive function better, as it is associated with less impairment of working memory and cognitive function.[18,19] However, few studies has evaluated the effect of surgery on mood status, cognitive function, and quality of life in patients with MTLE. Therefore, we assessed changes in these characteristics after anterior temporal lobectomy in a single-arm cohort study of patients with MTLE.
This study was approved by the Ethics Committee of Xuanwu Hospital. The requirement for informed consent was waived due to the retrospective design of the study.
This single-arm cohort study examined cognitive function, mood status, and quality of life, as well as electroencephalography (EEG) findings, in patients who underwent anterior temporal lobectomy at Xuanwu Hospital from January 2018 to March 2019. Assessments and EEG were performed in each patient before surgery and 12 months after and then compared these findings to evaluate the effect of surgery. Engel Epilepsy Surgery Outcome Scale scores were evaluated based on the follow-up record of epilepsy episodes.
Patients who met the following criteria were considered eligible for study inclusion: (1) Aged 18 to 55 years; (2) Epilepsy diagnosed and classified according to the standards of the International League Against Epilepsy; (3) Minimum 6 years of education; (4) Receipt of ≥2 antiepileptic drugs for no less than 2 years; seizures occurring no less than 4 times each year; (5) Diagnosis of unilateral temporal epilepsy based on a comprehensive evaluation of symptoms, sphenoidal node EEG, MRI, and positron emission tomography, or magnetic EEG; hippocampus atrophy evident on MRI; (6) EEG showing unilateral or predominantly (>75%) lateralized anterior temporal spike discharges during the interictal period with maximal ipsilateral rhythmic activity over the anterior temporal or subtemporal region during the ictal period; (7) Agreeing to provide consent to participate.
Patients with the following conditions were excluded: (1) Symptomatic epilepsy induced by stroke, trauma, or hypoparathyroidism; (2) Severe depression or anxiety (Self-Rating Anxiety Scale [SAS] score >69, Self-Rating Depression Scale [SDS] score >73); (3) Epilepsy caused by regional cortical dysplasia, angioma, or brain tumor; (4) Recent use of medications with side effects of cognitive-affecting, including topiramate, phenobarbital, and phenytoin sodium; recent history of sedative or hypnotic medication, including benzodiazepines and other anti-depressants; (5) Severe cardiopulmonary dysfunction, progressive central nervous system disease, cognitive impairment, and psychiatric disorders; (6) Heavy alcohol consumption; (7) Bilateral epileptogenic lesions confirmed by EEG or bilateral hippocampus sclerosis detected on MRI; (8) Previous history of craniotomy; (9) Inability to complete follow-up and questionnaire surveys; (10) Previous diagnosis of inherited epilepsy or epileptic encephalopathy, including Ohtahara syndrome, early myoclonic encephalopathy, Dravet syndrome, infantile spasms, Lennox–Gastaut syndrome, Angelman syndrome, and Doose syndrome.
Cortico-amygdalohippocampectomy (CAH) involving resection or disconnection of the temporal pole and temporal neocortex and resection of the amygdala and hippocampus was performed in all patients. All surgeries were performed by one of two neurosurgeons experienced in epilepsy surgery. The extent of lateral neocortical disconnection/resection as measured from the anterior tip of the temporal pole was approximately 4 cm in the language-dominant hemisphere and 6 cm in the non-dominant hemisphere. For CAH of the dominant hemisphere, the language areas were mapped using a standard electrical stimulation protocol. The superior temporal gyrus was preserved accordingly in some dominant hemisphere cases. The extent of hippocampal resection was tailored according to intraoperative electrocorticography and ranged approximately 1 to 4 cm as measured from the head of the hippocampus. The extent of the lateral and mesial resection/disconnection was also tailored according to intraoperative electrocorticography.
Patient characteristics and demographics were recorded by attending physicians. The following epilepsy-related data were also recorded: (1) Birth information, family history, and history of trauma, surgery, cerebritis, or other pathological brain disorder. (2) Initial seizure episode, course and type of seizures, episode frequency (per month), and duration. (3) Current medications, including dose and timing of administration. (4) Severity of hippocampal atrophy as assessed by pre-operative MRI: obvious atrophy was graded class I; widened choroidal fissure only was graded class II; mild-to-moderate hippocampal volume reduction was graded class III; severe hippocampal volume reduction was graded class IV. (5) Histopathological examination of surgical specimens after hematoxylin-eosin staining was conducted independently by two experienced pathologists.
Video-assisted EEG was independently interpreted by two neuro-electrophysiologists. One awake and one sleep phases, every 30 minutes in duration, were randomly selected for interpretation. The number of epileptic waves (including spike waves, sharp waves, high-amplitude slow waves, and spike-and-slow waves) was counted in each phase, and the mean number of epileptiform discharges for the two phases was recorded for each patient. Change in the number of epileptiform discharges post-operatively was calculated as follows: (pre-operative epileptiform discharges – post-operative epileptiform discharges)/pre-operative epileptiform discharges × 100%.
Cognitive function assessment
Cognitive function was assessed by a neurologist trained and experienced in neuropsychology using several neuro-psychology assessment tools. The Mini-Mental State Examination (MMSE) was used to assess capabilities in orientation, memory, concentration, calculation, and verbal ability.
The Boston Naming Test (BNT) was used to measure confrontation naming. Test participants were asked to name 60 line-drawn graphics graded according to familiarity. Standard stimulus prompts and voice prompts were given if the graphic could not be named. The number of correct named graphics was the final score.
The Montreal Cognitive Assessment (MoCA) was used to assess cognitive function in eight domains: concentration, executive function, memory, language, visualized structural ability, abstract thinking, calculation, and orientation. The final scores were adjusted for education; one point was added to the scores of subjects with ≤12 years of education.
Mood status assessment
Mood status was evaluated by the patients themselves and by two trained investigators through conversation and observation. Depression was evaluated with the SDS and Hamilton Depression Rating Scale (HAMD).[25,26] Anxiety was evaluated with the SAS and Hamilton Anxiety Rating Scale (HAMA).[27,28] Investigator scores were first determined by each investigator independently; a unified final score for each patient was then determined by consensus after discussion.
Quality of life assessment
Study participants completed the Quality of Life in Epilepsy (QOLIE-31) survey under investigator guidance. The revised QOLIE-31 scale includes 33 items in eight domains of living status: worry about seizures (five items); general health level (two items); emotional health (five items); energy/fatigue (four items); cognitive function (six items); drug impact (three items); social function (seven items); and comprehensive quality of life (one item). The initial score in each domain was calculated as the sum of the scores divided by the number of items in the domain. The total score was then derived by a weighted sum of the scores from each domain. Higher scores indicate better quality of life.
Post-operative seizure outcome was measured using the Engel Epilepsy Surgery Outcome Scale using data recorded by patients and one or two family members in a seizure record book. Recorded data included date of onset, triggers, aura, manifestations, duration, post-onset status, and medication status.
Statistical analyses were performed using SPSS version 22 (IBM, Armonk, NY, USA). Shapiro–Wilk test was used for normality test. Quantitative data are presented as means with standard deviation or medians with interquartile range depending on normality of distribution. The independent t-test or Mann-Whitney U test was used as appropriate to compare pre- and post-operative data. The χ2 test was used to compare categorical data. All tests were two-tailed. P < 0.05 was considered statistically significant.
Patient characteristics are presented in Table 1. A total of 31 patients were enrolled in the study: 18 (58.1%) men and 13 (41.9%) women. The mean patient age at the time of initial seizure was 16.61 years ± 9.28 years. The mean duration of illness was 11.97 years ± 8.29 years. The median number of medications, episodes per month, and years of education was 3, 9, and 8, respectively. Then, 18 patients reported generalized onset tonic-clonic seizure secondary to focal onset seizure; 25 patients reported focal onset seizure with impaired awareness; and 12 reported focal onset seizure with patent awareness. Most patients (56.6%) reported mixed types of episodes.
Table 1 -
Characteristics of study participants (n
|Age at operation (years)
||29.10 ± 6.95
|Age of initial episode (years)
||16.61 ± 9.28
|Course for illness (years)
||11.97 ± 8.29
|Numbers of medication
||3 (2, 3)
|Frequency of outbreaks (per month)
||9 (9, 12)
||8 (6, 12)
|Types of seizure
| GTCS, SPS, CPS
| GTCS, CPS
| GTCS, SPS
| Hippocampal sclerosis
| Temporal lobe softening
| No specific pathological changes
Data are presented as n (%), median (interquartile range) or mean ± standard deviation. CPS: Complex partial seizure; GTCS: Genralized tonic- clonic seizure, SPS: Simple partial seizure.
Pre-operative EEG detected unilaterally initiated temporal lobe spikes, spike waves, sharp waves, and sharp slow waves in all patients, indicating seizure origin in the temporal lobe; epileptiform discharges became generalized in some cases. Epileptiform discharges were detected on sphenoid electrodes in 30 of 31 patients and detected during sleep in 26 patients. MRI showed grade I–II hippocampal atrophy in 19 patients and grade III–IV atrophy in 12. All epileptogenic lesions were located in the mesial temporal lobe. Post-operative pathological examination detected hippocampal sclerosis in 24 patients, glial hyperplasia in two, temporal lobe softening in one, and non-specific changes in four [Table 1].
Surgical specimens from each patient underwent pathological examination. Hippocampus sclerosis was found in 24 (77.4%) cases, softening lesions within the temporal lobe were found in one (3.2%), glial proliferation was found in two (6.5%), and non-specific findings were found in four (12.9%, n = 31).
As shown in Table 2, MMSE, MoCA, and BNT scores did not significantly change from before surgery to 12 months after. When MoCA subdomains were compared, significant increases in visuospatial ability and abstract thinking scores were detected while language ability scores significantly decreased.
Table 2 -
Comparisons of pre- and post-operative cognitive functions of participants pathological outcomes.
|Total (n = 31)
||21 (20, 26)
||23 (21, 26)
||22 (21, 26)
||23.03 ± 2.57
||19 (17, 23)
||20 (18, 22)
|| Visuospatial ability
||3.87 ± 0.86
||4.13 ± 0.89
||4 (3, 5)
||3 (3, 4)
|| Concentration and calculation
||3 (3, 5)
||4 (3, 5)
|| Abstract thinking
||1 (1, 2)
||2 (1, 2)
|| Delayed recall
||2 (1, 3)
||1 (1, 2)
||4 (3, 5)
||4 (4, 5)
|Dominant side (n = 15)
||22.00 ± 4.55
||21.88 ± 3.32
||19.25 ± 4.88
||18.69 ± 3.34
||22.44 ± 3.03
||22.00 ± 1.83
|Non-dominant side (n = 16)
||22.53 ± 2.80
||24.27 ± 2.57
||19.40 ± 3.27
||20.80 ± 3.30
||23.47 ± 3.23
||24.13 ± 2.85
Data are presented as mean ± standard deviation or median (interquartile range). BNT: Boston Naming Test; MMSE: Mini-Mental State Examination; MoCA: Montreal Cognitive Assessment.
The left hemisphere was considered dominant in all patients since all were right-handed and Wada testing was not performed. We observed that the laterality of language as determined by intraoperative electrical cortical stimulation was consistent with the dominant hemisphere as determined by traditional right handedness. Fifteen patients underwent dominant lobectomy. The MoCA score significantly decreased slightly post-operatively in these patients while MMSE and BNT scores remained unchanged. For the 16 non-dominant lobectomy patients, all three scores increased; however, the increase was significant only for MMSE scores [Table 2].
At 12 months post-operatively, in patients with the dominant side temporal lobe resection, verbal memory deficits and diminished ability for naming items were observed (P < 0.05) [Table 3].
Table 3 -
Comparison of pre- and post-operative MoCA subdomains in patients with the dominant side temporal lobe resection.
||4.00 (3.25, 5.00)
||4.00 (4.00, 5.00)
|Language and naming ability
||4.50 (3.00, 5.00)
||3.50 (2.25, 4.00)
|Concentration and calculation
||4.0 (3.0, 5.0)
||4.5 (3.0, 5.0)
||1.5 (1.0, 2.0)
||2.0 (1.0, 2.0)
||2.0 (1.0, 3.0)
||1.0 (1.0, 2.0)
||43.25 (4.00, 5.00)
||1.00 (1.00, 2.00)
Data are presented as median (interquartile range). MoCA: Montreal Cognitive Assessment.
Mood status and quality of life
As shown in Table 4, pre- and post-operative scores of the SAS (46.84 ± 7.95 vs. 42.68 ± 7.70), SDS (37.94 ± 7.51 vs. 32.81 ± 9.84), HAMA (12.06 ± 1.99 vs. 9.13 ± 2.31), and HAMD (11.13 ± 3.30 vs. 8.42 ± 2.61) were significantly different and improved post-operatively (P < 0.05). The QOLIE score (58.23 ± 7.58 vs. 69.77 ± 10.30), including all domain subscores other than cognition, also improved post-operatively.
Table 4 -
Comparisons of pre- and post-operative mood status
and quality of life in participants.
||12.06 ± 1.99
||9.13 ± 2.31
||11.13 ± 3.30
||8.42 ± 2.61
||46.84 ± 7.95
||42.68 ± 7.70
||37.94 ± 7.51
||32.81 ± 9.84
|Quality of life
||58.23 ± 7.58
||69.77 ± 10.30
| QOLIE-31 score
||58.23 ± 7.58
||69.77 ± 10.30
| Concerns of seizures
||38.61 ± 4.87
||62.10 ± 13.07
| Overall quality of life
||59.87 ± 3.96
||64.00 ± 8.63
||45.55 ± 7.20
||60.74 ± 7.62
||52.90 ± 6.84
||66.65 ± 13.18
||53.26 ± 7.14
||51.58 ± 8.31
| Adverse effect
||58.19 ± 5.33
||77.32 ± 10.07
| Social activity
||55.77 ± 5.73
||66.35 ± 8.22
| General health status
||61.61 ± 6.38
||72.90 ± 6.93
HAMA: Hamilton Anxiety Rating Scale; HAMD: Hamilton Depression Rating Scale; QOLIE-31: Quality of Life in Epilepsy; SAS: Self-Rating Anxiety Scale; SDS: Self-Rating Depression Scale.
EEG examination showed that 29 patients exhibited a lower rate of epileptiform discharges post-operatively, resulting in a reduced rate of 71.9%. Post-operative Engel classification was as follows: class I, 14 patients; class II, ten patients; class III, five patients; and class IV, two patients. The overall success rate of surgery (Engle class I–II outcome) was 77.4%.
In this study, 31 patients with MTLE underwent CAH without major complications. Although CAH did not cause significant changes in cognitive function overall, changes were detected in some cognitive functions, including visuospatial ability, executive ability, and abstract thinking. Hippocampus sclerosis was the predominant pathological finding. CAH resulted in improved anxiety and depression symptoms and reduction in the number of epileptic discharges. The overall success rate of surgery was acceptable.
A favorable outcome after CAH as measured by the Engel scale (Engel class I–II) was achieved in 78% of patients in this study; 45% were free of disabling seizures (Engel class I). A recent study also found that additional temporal lobe resection had favorable effects in some patients with cavernous malformations. Although many studies have emphasized that selective resection is associated with better preservation of cognition function and working memory, whether this applies to patients with MTLE has remained unknown.[32-34] Selective surgery should be selected as treatment after careful pre-operative evaluation, as the goal of surgery is to control recurrence of epileptiform discharges and prevent further damage to brain function. In contrast to previous studies, we examined post-operative EEG, which might be valuable in evaluating patients with MTLE post-operatively. Our surgical pathological finding that hippocampus sclerosis was the predominant lesion is consistent with pre-operative imaging studies and in agreement with the findings of Duarte et al.
There was no significant difference in cognitive scores between the pre-operative and post-operative evaluations at 12 months post-operatively. However, visuospatial ability, nomenclature, executive ability, and abstract thinking improved post-operatively, whereas language and naming abilities were significantly impaired. The postoperative declines in language and naming ability as well as recall may be related to resection of related functional areas, as the efferent fibers of the hippocampus participate in advanced neural activities such as learning, memory, and emotion via the Papez loop. The amygdala is involved in cognitive memory, memory connections, and visceral, endocrine, and emotional activities, all of which can be affected by surgical resection. Language function in some patients decreased significantly post-operatively, which was more likely in patients with dominant lobectomy, particularly declined naming ability; this finding is consistent with a previous study by Jehi et al. Memory changes before and after the operation may be related to compensation by the contralateral hippocampus. If contralateral compensation is adequate before surgery, there is generally no significant postoperative memory function loss. Anterior temporal lobe damage, particularly the left anterior temporal lobe, may aggravate declines in naming ability and semantic understanding, which have a great impact on learning and memory. A previous functional MRI study of patients who underwent anterior temporal lobectomy demonstrated that bilateral anterior temporal lobe damage can cause a severe decline in semantic function; however, unilateral atrophy/resection has a limited effect. Two mechanisms can potentially improve resistance to unilateral temporal injury: complete compensation by upregulation of the contralateral temporal lobe and compensation by the anterior frontal area controlled by semantic retrieval.[40,41] Therefore, unilateral anterior temporal lobectomy has a smaller effect on semantic cognition function because of bilateral brain network compensation.
Repeated synchronous discharge of brain neurons in patients with MTLE may cause damage to functional areas of the brain. MTLE on the dominant side is usually associated with impaired speech, learning, and short-term or working memory. MTLE on the non-dominant side can predispose to disorders of spatial memory, facial recognition, and expression recognition. When a general tonic-clonic seizure occurs, the function of the frontal lobe may also be impaired. TLE lesions can cause functional impairment of the anterior temporal structures responsible for semantic processing and the posterior neocortical structures responsible for lexical processing. In this study, the post-operative MMSE and BNT scores were lower in dominant patients with MTLE than in nondominant patients at 1 year, indicating that dominant-side surgery is more likely to result in cognitive impairment. The MMSE score in dominant patients with MTLE was lower 1 year post-operatively than that before. However, both MMSE and MoCA scores in non-dominant patients with MTLE significantly improved. Previous studies have shown that patients undergoing dominant anterior temporal lobectomy are prone to verbal memory impairment, whereas those undergoing non-dominant lobectomy are prone to impairment of visual memory and other non-verbal memory, which can be discriminated by functional MRI.[43,44] Another study reported that average speech memory declined in 44% of patients undergoing left-side surgery and 20% of right-side surgery patients; at the same time, approximately 34% of left-side surgery patients experienced difficulties with nomenclature. Verbal memory studies after anterior temporal lobectomy have shown that post-operative memory score is lower in dominant-side surgery and side is an independent predictor of post-operative language memory decline.[46,47] Taken together, these results suggest that side of surgery and individual pre-operative cognitive function should be considered when performing anterior temporal lobectomy.
Anxiety, depression, egocentrism, and abnormal thinking patterns can be seen in patients with MTLE. Those with refractory MTLE often have anxiety and depression, typically mild to moderate in severity. Among the 31 patients in this study, 95.3% had possible anxiety (HAMA score >7) and 84.9% had possible depression (HAMD score >7). HAMA, SAS, HAMD, and SDS scores at 1-year post-operative follow-up were significantly lower than those before surgery. Improved mood post-operatively is related to the reduction in degree and frequency of seizures and absence of cognitive decline. A small number of patients may have disturbed mood because of the double blow of post-operative epilepsy and memory decline. However, we found that depression and anxiety scores improved post-operatively in general. Thus, future studies are needed to identify patients likely to experience mood benefits from surgery.
Declined quality of life in patients with refractory MTLE is related to many factors, including uncontrollable seizures, young age of onset, long disease course, and side effects of AED drugs, such as depression, anxiety, and cognitive impairment. The main purpose of epilepsy treatment is to improve the quality of life to an acceptable level. Post hoc analysis of the various parameters in the QOLIE-31 before surgery and 1 year after demonstrated significant increases in anxiety, overall quality of life, mood, energy, drug side effects, social activities, and overall health. Compared with healthy people, emotion recognition in TLE patients is significantly impaired, particularly for negative emotions (fear, disgust, sadness, and anger), which may be linked to a decline in social ability. The amygdala plays a crucial role in facial expression recognition. McClelland and Jaboin found that anterior temporal lobectomy does not impair facial expression recognition. Shaw et al found that the ability to recognize fearful facial expressions in patients was enhanced after left anterior temporal lobectomy and may be closely related to right amygdala compensation. Post-operative intermittent seizures rarely have an impact on social function. In our QOLIE-31 subanalysis, we found that social activity improved post-operatively, which may be related to improved facial emotion recognition. Further studies are needed to elucidate the links between social ability, facial emotion recognition, and epilepsy surgery in patients with MTLE.
There are several limitations of this study. First, the improvement in other cognitive domains in this study may have been due to the existence of a small gap in the scores of the subdomain scales, low sensitivity of the scoring tests, and the learning and memory contents of the tests. Second, the cognitive tests were subject to patient capacity and understanding. Finally, we did not apply functional MRI data in our analyses.
This study demonstrated that CAH is safe and results in control of seizures and improvement in mood status and quality of life in patients with MTLE without significantly affecting cognitive function.
Conflicts of interest
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