Research Article, J Neurosci Clin Res Vol: 9 Issue: 1
Influence of a Slight Damage to the Mesial Temporal Lobe Visible on Positron Emission Tomography on Severity of Cognitive Impairment and Course of Epilepsy
Jacek Mądry*, Karolina Duszyńska Wąs, Agnieszka Drzewińska, Hanna Grygarowicz and Andrzej Friedman
1Department of Neurology, Brodnowski Hospital, Medical University of Warsaw, Warsaw, Poland
*Corresponding Author: Jacek Mądry,
Department of Neurology, Medical
University of Warsaw, Warsaw, Poland
Tel:+48 609-293-612
E-mail: jacekmadry@wp.pl
Received Date: 08 January, 2024, Manuscript No. JNSCR-24-124684;
Editor assigned Date: 10 January, 2024, Pre QC No. JNSCR-24-124684 (PQ);
Reviewed Date: 24 January, 2024, QC No JNSCR-24-124684;
Revised Date: 31 January, 2024, Manuscript No JNSCR-24-124684 (R);
Published Date: 07 February, 2024, DOI: DOI: 10.4172/Jnscr.1000178.
Citation: Mądry J et al. (2024) Influence of a Slight Damage to the Mesial Temporal Lobe Visible on Positron Emission Tomography on Severity of Cognitive Impairment and Course of Epilepsy. J Neurosci Clin Res 9:1.
Abstract
Aim: The study on the influence of minor lesions of the mesial temporal lobe visible on positron emission tomography on the severity of cognitive disorders and the course of epilepsy.
Material and Methods: A group of thirty one patients with mesial temporal lobe epilepsy of unknown cause, mild course and positive response to treatment was divided into a group of fifteen patients with reduced uptake of the 18F-fluorodeoxyglucose tracer and a group of sixteen patients with normal uptake of this tracer from mesial temporal lobe shown on positron emission tomography. Then, the two groups were compared in terms of the severity of cognitive impairment and the course of epilepsy. The group of fifteen patients with reduced uptake of the 18F-fluorodeoxyglucose tracer from the mesial temporal lobe, was later divided into a group of five patients who had indistinct mesial temporal sclerosis shown on magnetic resonance imaging and a group of ten patients who had visible changes only on positron emission tomography. They again underwent the above mentioned comparison.
Results: In the first comparison, there were significantly bigger cognitive impairments in the range of functions of attention p=0,037 and the sum of individual cognitive functions was p=0,032. In the second comparison bigger cognitive impairments were noticed in the range of verbal memory p=0,032, the overall Behavioral Assessment of the Dysexecutive Syndrome-score was p=0,015 and executive functions were p=0,011. There were no significant differences in the course of epilepsy.
Conclusions: A slight damage to the mesial temporal lobe visible on positron emission tomography or slightly larger damage to the mesial temporal lobe cause significantly bigger cognitive impairment, without a clear impact on the severity of epilepsy. The obtained results contradict the characteristics of benign mesial temporal lobe epilepsy
Keywords: 18F-Fluorodeoxyglucose marker; Positron emission tomography; Cognitive impairment
Introduction
There are discrepancies in the assessment of the presence of cognitive impairment in patients with Mesial Temporal Lobe (MTL) epilepsy who respond positively to antiepileptic drug treatment, who show regressing seizure frequency and no distinct changes in these brain structures on Magnetic Resonance Imaging (MRI). There is an opinion that cognitive disorders do not necessarily occur in patients with the mild form of this epilepsy.
Epilepsy from the mesial temporal lobe with MTL sclerosis visible on MRI, which is resistant to treatment, is better known. Researchers generally agree that the patients with severe epilepsy from mesial temporal lobe usually have cognitive impairment, mainly in the field of verbal and visual memory. Sclerosis is a process involving the loss of neurons in certain brain structures with secondary glial proliferation in this area. Usually it is unilateral, in 80% of cases [1-3]. It may be genetically determined or evoked by micro-trauma, febrile seizures in early childhood as well as by an infection of the central nervous system at a later age [1,4].
Positron Emission Tomography and Computed Tomography (PET/CT) is a more sensitive test for finding small lesions in the brain, including the mesial temporal lobe, than MRI examination [5,6]. PET/CT of the head in the inter ictal phase shows reduced cerebral flow in the epileptic focus and decreased metabolism of 18F-fluorodeoxyglucose marker in these brain structures [7-9]. PET/ CT does not show the type of pathological process in the damaged areas of the brain. The seen in the MTL changes may come from sclerosis, micro-dysgenesis, and Focal Cortical Dysplasia (FCD) [10,11]. In order to find all minor brain changes and determine their nature, the patient should undergo MRI and PET/CT examinations.
The term FCD is misleading because very small, often microscopic lesions also occur in other parts of the brain, not only in the cortex [10-12]. FCD of the first type is often congenital. It does not damage the architecture of the brain structures and is usually invisible in imaging tests [10,13]. Micro-dysgenesis is also a minor lesion, but still it can damage the architectures of the brain [2,9]. The sclerosis can occur with or without FCD. It can be indistinct, and it can only damage the mesial temporal lobe. Extensive sclerosis clearly visible on MRI is a significant brain damage [14,15].
Some researchers believe, that patients suffering from mesial temporal lobe epilepsy with a mild or even slightly more severe course, may have no memory or other cognitive disorders. This problem was presented in details by Suresh et al., [16]. Their eighteen patients had no sclerosis from mesial temporal lobe visible on MRI though they had quite severe course of epilepsy. In the cases of these patients no memory impairments were detected in the conducted psychological tests.
The authors describing the so-called Benign Mesial Temporal Lobe Epilepsy (BMTLE), claim that even during the period of occurrences of epileptic seizures, patients with this type of epilepsy did not have noticeable cognitive disorders [1,17,18]. The patients with the diagnosed BMTLE must be seizure-free for at least 24 months. Epileptic seizures can withdraw as the result of treatment with antiepileptic drugs or spontaneously [1]. Among the patients suffering from benign mesial temporal lobe epilepsy, in 40% of cases, as MRI shows, sclerosis was found in these structures of the brain [1,14,15,17,18].
The whole, current study attempts to dispel doubts regarding the occurrence of cognitive disorders in patients with mild course of mesial temporal lobe epilepsy. It was analyzed how microscopic damage of mesial temporal lobe causes the appearance of noticeable cognitive disorders. It was also studied if in a completely mild epilepsy already occur selective, but noticeable cognitive disorders. According to our knowledge, such a detailed analysis was missing in medical literature [19,20].
Materials and Methods
The study group consisted of thirty one patients, suiting numerous requirements, was chosen from a larger group. Patients were over 18 years old. They had been suffering from mild to moderate epilepsy from the mesial temporal lobe for many years. They also responded positively to AEDs. They reported slight difficulties in longer utterances, in remembering, and functions of attention [21-23].
There were also exclusion criteria such as:
• Known causes of epilepsy such as perinatal trauma, later serious head injury, tumor or stroke, previous encephalitis and meningitis,
• Large damage to the mesial temporal lobe clearly visible on MRI of the head,
• Pronounced cognitive impairment (disqualified patients scored fewer than 26 points by solving the Mini-Mental State Examination-MMSE),
• Depressive disorders,
• Patients suffering from diabetes and diseases causing liver or kidney failure.
Each patient underwent MRI of the head on the 1,5 Tesla apparatus, PET/CT using an 18F-FDG marker as well as electroencephalography at rest and after a sleepless night. All tests were performed on the same equipment. Each patient had a detailed examination of individual cognitive functions and also had a blood test.
In detailed interviews each patient confirmed the onset of seizures, duration of the disease and frequency of epileptic seizures in the last year.
EEG abnormalities were calculated on the basis of a five-point scale. The scale was developed in order to standardize and compare the EEG test results of patients from the study group.
• There were no EEG abnormalities.
• Single slow theta waves, less often delta waves, very rarely sharp waves and spikes occasionally appeared in the pretemporal leads or later in the rest of the temporal lobe.
• Abortive sharp waves with a slow delta waves or less often spikes with a slow delta waves appeared in the pre-temporal leads or later in the rest of the temporal lobe.
• The tendency to generalize-theta waves or, less frequently, delta waves with emerging sharp waves or single spikes spread from the temporal lobe to some other leads, more unilateral.
• Incomplete generalization-sharp waves or sometimes spikes or complexes of a sharp waves with a slow delta waves or spikes with a slow delta waves originating in the temporal lobe spread to some other leads. There was no case of complete generalization.
The study on learning, verbal memory and visual memory was carried out using two independent tests: California Verbal Learning Test (CVLT) and Rivermead Behavioral Memory Test (RBMT)- Third Edition.
The study of other cognitive functions was performed with: The Wechsler Adult Intelligence Scale Revised-(WAIS-R), Individual Verbal Fluency Tests, Test Judgement of Line Orientation-connecting lines with each other - (Test Benton JLO), and Behavioral Assessment of the Dysexecutive Syndrome - (BADS) were used to assess cognitive functions. The BADS test consists of five individuals, independent sub-tests: changing of the rule, programming the operation, ZOO map, looking for a key and 6-elements.
Individual tests and subtests were grouped to examine: Memory and learning, visual-spatial, executive, and attention functionsthat is, the main cognitive functions. Later, tests and subtests of cognitive functions were standardized in order to perform statistical calculations, according to the following division:
• Patients without a cognitive deficit.
• Patients with mild cognitive deficit.
• Patients with cognitive impairment.
Basing on the PET/CT results, the group of thirty one patients was divided into 15 patients with reduced uptake of the 18F-FDG tracer and 16 patients with normal uptake of this tracer from the mesial temporal lobe. These two groups of patients were compared in the terms of the severity of cognitive impairment and the onset of seizures, duration of the disease, frequency of epilepsy seizures, the percentage difference in the size of the hippocampus, pathological changes in resting electroencephalography and after sleepless night. The level of the patients’ education was also compared. Then, the group of fifteen patients with reduced uptake of the 18F-FDG tracer from the mesial temporal lobe was divided into a subgroup of five patients with already indistinct sclerosis shown on MRI and a subgroup of ten patients with changes in the brain structures shown only on PET/CT. The same comparison as before was made in the second case. All calculations were repeated twice.
Results and Discussion
In the subgroup with visible indistinct sclerosis in the mesial temporal lobe shown on MRI there was no tendency towards bigger changes shown in EEG, worsening of the course epilepsy and there was no clear difference in the patients’ level of education (Tables 1-4). The patients in the current research work felt slight cognitive disorders but had some difficulties with explaining them. Such a small cognitive deficit was hardly noticeable during ordinary daily activities. Cognitive disturbances appeared clearer only while performing more difficult tasks. Some difficulties emerged during longer, more detailed utterances. Due to the mentioned above problems some patients often lost more advanced, permanent jobs. They needed more time to prepare for more demanding exams.
| Dependent variables (Study of cognitive functions) | Patients with normal uptake of the 18F-FDG tracer from the mesial temporal lobe shown on PET/CT. (n=16) | Patients with reduced uptake of the 18F-FDG tracer from the mesial temporal lobe shown on PET/CT. (n=15) | p | ||
|---|---|---|---|---|---|
| Mean | Standard deviation | Mean | Standard deviation | ||
| WAIS-R repeating digits Sub-test | 1,13 | 0,342 | 1,13 | 0,352 | 0,946 |
| CVLT-1 sub-test | 1,31 | 0,704 | 1,87 | 0,915 | 0,056 |
| Attention function (WAIS-R repeating digits+CVLT-1) | 1,25 | 0,577 | 1,60 | 0,507 | 0,037 |
| Verbal fluency (k+ p+ animals) | 1,44 | 0,629 | 1,53 | 0,640 | 0,634 |
| Overall BADS test results | 1,13 | 0,342 | 1,47 | 0,640 | 0,078 |
| Executive functions (Verbal fluency+BADS) | 1,38 | 0,500 | 1,67 | 0,617 | 0,177 |
| Visual-spatial functions (Benton JLO Test) | 1,06 | 0,250 | 1,13 | 0,352 | 0,512 |
| Visual memory (RBMT) Sub-tests: RBMT-pictures, RBMT-facies; RBMT-direct learning; RBMT-learning after postponement | 1,50 | 0,516 | 1,80 | 0,775 | 0,294 |
| Verbal memory (CVLT). Sub-tests: CVLT-5, CVLT-PFLP, CVLT-PHLP | 1,06 | 0,250 | 1,33 | 0,617 | 0,122 |
| Verbal memory (RBMT). Sub-tests: RBMT-direct history, RBM-postponement history, RBMT-facies and names. | 1,25 | 0,447 | 1,60 | 0,632 | 0,095 |
| Global score of cognitive functions: Attention, executive, visual-spatial functions, visual memory (RBMT), verbal memory (CVLT), verbal memory (RBMT). | 1,44 | 0,512 | 1,87 | 0,516 | 0,032 |
Note: WAIS-R=Digit repetition; the patient repeats a sequence of digits that he heard previously; CVLT-1; the patient repeats what he heard after the first attempt; Function of attention-sum of sub-tests WAIS-R+CVLT-1; Verbal fluency: category the letter p, the letter k and the names of the animals; BADS-total score: the sum of the results from five sub-tests; Executive Functions-sum of sub-tests of Verbal Fluency+BADS total score. Visual-Spatial Functions-on the basis of the Benton-JLO test; Learning and visual memory RBMT. Total score; the sum of the results of RBMT-pictures, RBMT-faces, RBMT-direct learning, RBMT-postponed learning; Learning and verbal memory CVLT. Total score; the sum of the results of CVLT-5, CVLT-PFLP, CVLT-PHLP; Learning and verbal memory RBMT. Total score; the sum of the results of RBMT-direct history, RBMT-postponed history, RBMT-names and surnames; Global score of cognitive functions: attention, executive, visual-spatial (functions), visual learning and memory (RBMT sub-tests), learning and verbal memory (CVLT sub-tests), learning and verbal memory (RBMT sub-tests).
Table 1: Comparison of the results of cognitive impairment tests in the group of patients with normal uptake and in the group with reduced uptake of the 18F-FDG tracer from the mesial temporal lobe shown on PET/CT.
| Dependent variables (Study of cognitive functions) | Patients with visible slight sclerosis of the mesial temporal lobe already shown on MRI and reduced uptake of the 18F-FDG tracer from MTL on PET/CT. (n=5) | Patients with only reduced uptake of 18F-FDG tracer from MTL shown only on PET/CT (n=10) | p | ||
|---|---|---|---|---|---|
| Mean | Standard deviation | Mean | Standard deviation | ||
| WAIS-R-repeating digits sub-test | 1,20 | 0,447 | 1,10 | 0,316 | 0,622 |
| CVLT-1 sub-test | 2,00 | 1,000 | 1,80 | 0,919 | 0,705 |
| Function of attention (WAIS-R-repeating digits+CVLT-1) | 1,60 | 0,548 | 1,60 | 0,516 | 1,000 |
| Verbal fluency (k+ p+ animals) | 1,80 | 0,447 | 1,40 | 0,699 | 0,269 |
| Overall BADS test results | 2,00 | 0,707 | 1,20 | 0,422 | 0,015 |
| Executive functions (Verbal fluency+BADS) | 2,20 | 0,447 | 1,40 | 0,516 | 0,011 |
| Visual-spatial functions Benton JLO Test | 1,20 | 0,447 | 1,10 | 0,316 | 0,622 |
| Visual memory (RBMT). Sub-tests: RBMT-pictures, RBMT-facies RBMT-direct learning RBMT-learning after postponement | 1,80 | 0,837 | 1,80 | 0,789 | 1,000 |
| Verbal memory (CVLT). Sub-tests; CVLT-5, CVLT-PFLP, CVLT-PHLP | 1,80 | 0,837 | 1,10 | 0,316 | 0,032* |
| Verbal memory (RBMT). Sub-tests; RBMT-direct history, RBMT-postponement history, RBMT-faces and names. | 2,00 | 0,707 | 1,40 | 0,516 | 0,082 |
| Global score of cognitive functions: attention, executive, visual-spatial functions, visual memory (RBMT), verbal memory (CVLT), verbal memory (RBMT). | 2,20 | 0,447 | 1,70 | 0,483 | 0,075 |
Note: WAIS-R-digit repetition; the patient repeats a sequence of digits that he heard previously; CVLT-1; the patient repeats what he heard after the first attempt; Function of attention-sum of sub-tests WAIS-R+CVLT-1; Verbal fluency: category the letter p, the letter k and the names of the animals; BADS – total score: the sum of the results from five sub-tests; Executive Functions-sum of sub-tests of Verbal Fluency+BADS-total score; Visual-Spatial Functions-on the basis of the Benton-JLO test; Learning and visual memory RBMT. Total score; the sum of the results of RBMT-pictures, RBMT-faces, RBMT-direct learning, RBMT-postponed learning; Learning and verbal memory CVLT.
Table 2: Comparison of cognitive impairment scores in smaller, isolated subgroups.
| The exponents of the course of epilepsy. Independent variables | Patients with normal uptake of the 18F-FDG tracer from mesial temporal lobe shown on PET/CT. (n=16) | Patients with reduced uptake of the 18F-FDG tracer from mesial temporal lobe shown on PET/CT. (n=15) | p | ||
|---|---|---|---|---|---|
| Mean | Standard deviation | Mean | Standard deviation | ||
| The beginning of onset | 20,56 | 18,301 | 24,33 | 18,415 | 0,593 |
| The duration of the disease | 19,19 | 12,101 | 23,13 | 16,724 | 0,429 |
| Dependent variables | (n=16) | (n=15) | p | ||
| Level of education | 3,56 | 0,512 | 3,13 | 0,640 | 0,059 |
| Frequency of epilepsy seizures | 1,88 | 0,885 | 2,07 | 0,884 | 0,641 |
| The percentage difference in the size of the hippocampus | 14,78 | 8,120 | 13.71 | 10,01 | 0,75 |
| The results of resting EEG-the examination of sum of pathological changes including generalizations | 2,69 | 1,448 | 3,20 | 1,373 | 0,319 |
| The results of EEG after a sleepless night the examination of sum of pathological changes including generalizations | 4,06 | 0,998 | 4,27 | 0,961, | 0,537 |
Note: Frequency of epilepsy seizures that took place the previous year. Abnormalities in resting EEG and EEG after a sleepless night. Calculations were based on a five –point scale described in the Materials and Methods chapter. Level of Education: The group of n=16: 9 Patients of higher education and 7 of secondary education. The group of n=15: 4 Patient of higher education, 9 of secondary education and 2 of vocational education.
Table 3: Comparison of test results determining the course of epilepsy in the group with normal uptake and in the group with reduced uptake of the 18F-FDG tracer from the mesial temporal lobe shown on PET/CT.
| The exponents of the course of epilepsy. Independent variables | Patients with visible slight sclerosis of the mesial temporal lobe already shown on MRI and reduced uptake of the 18F-FDG tracer from MTL shown on PET/CT. (n=5) | Patients with only reduced uptake of 18F-FDG tracer from MTL shown only on PET/CT (n=10) | p | ||
|---|---|---|---|---|---|
| Mean | Standard deviation | Mean | Standard deviation | ||
| The beginning of onset | 39,8 | 25,282 | 21,5 | 14,308 | 0,668 |
| The duration of the disease | 27,4 | 21,090 | 21,0 | 14,907 | 0,423 |
| Dependent variables | (n=5) | (n=10) | p | ||
| Level of education | 3,00 | 0,548 | 3,00 | 0,667 | 0,963 |
| Frequency of epilepsy seizures | 1,80 | 0,837 | 2,20 | 0,919 | 0,397 |
| The percentage difference in the size of the hippocampus | 18,67 | 15,130 | 11,74 | 7,311 | 0,396 |
| The results of resting EEG-the examination of the sum of pathological changes including generalizations | 3,20 | 1,643 | 3,20 | 1,317 | 0,948 |
| The results of EEG after a sleepless night the examination of the sum of pathological changes including generalizations | 4,20 | 0,837 | 4,30 | 1,059 | 0,638 |
Note: Frequency of epilepsy seizures that took place the previous year. Abnormalities in resting EEG and EEG after a sleepless night. Calculations were based on a five –point scale described in the Materials and Methods chapter. Level of education: The group of (n=10): Patients of higher education 2, secondary education 6 and vocational education.2 The group of (n=5): Patients of higher education 2, secondary education 3.
Table 4: Comparison of test results determining the course of epilepsy in smaller, isolated subgroups.
The results of the analyses carried out in the current work clearly indicate that epilepsy from the mesial temporal lobe always coexists with slight, selective cognitive disorders, even in the cases when patients do not have any abnormalities visible on MRI and PET/CT images of these brain structures. The examined patients with slight changes in the mesial temporal lobe visible on PET/CT already had statistically, significantly bigger cognitive impairments in the range of function of attention. Their sum of individual cognitive functions was also statistically, significantly bigger compared to the patients without any visible changes in MTL. These were not attention disorders caused by depressed mood, because patients suffering from depression were not included in the study group. In the next analyses, the patients with indistinct sclerosis of mesial temporal lobe already visible on MRI and coexisting lesions detected on PET/CT were compared with the patients with lesions in brain structures visible only on PET/CT.
The difference in the size of mesial temporal lobe damage between the subgroup of patients with indistinct sclerosis in MTL visible on MRI was only slightly bigger compared to the subgroup of patients with changes visible only on PET/CT. However, there were statistically significantly bigger disturbances in the range of verbal memory, the overall BADS test and executive functions in the examined patients. This contradicts with some statements in the medical literature. Suresh et al., described patients who had quite severe epilepsy from the mesial temporal lobe but had no confirmed memory disorders. It must be emphasized that in Suresh et.al. Research work, the patients underwent only two Individual neuropsychological tests.
There are also other scientific articles in which the conclusions were drawn on the basis of a neuropsychological examination performed with a single test. The characteristics of BMTLE raise the greatest doubts. It is believed that patients with BMTLE have no noticeable cognitive impairment, although nearly half of them have sclerosis in the mesial temporal lobe visible on MRI.
This means that patients with a clear damage to the brain structures responsible for memory and learning do not even have selective cognitive impairment. This is utterly improbable. The study of cognitive functions should be carried out in a holistic manner, because individual cognitive functions are to some extent interrelated. Comprehensive examination of cognitive functions enables discovery of disturbances that are not as specific to the MTL location as executive functions disorders. Some cognitive functions should be assessed by two independent psychological tests. Only such an examination can reveal slight, selective cognitive disorders and then, so small change in cognitive functions would be shown in a completely mild form of epilepsy from mesial temporal lobe.
In the current study, research was also conducted on the impact of minor damage to the mesial temporal lobe on the course of epilepsy. Basing on the results obtained in these analyses, there was no significant intensification of the course of epilepsy due to the appearance of such small changes in the mesial temporal lobe.
Conclusion
A slight damage to the mesial temporal lobe visible on PET/CT or a slightly larger damage to the MTL causes significantly bigger cognitive impairment without showing any significant impact on the severity of epilepsy. The obtained result contradicts the characteristics of benign mesial temporal lobe, because 40% of patients with BMTLE who have distinct sclerosis in the mesial temporal lobe found on MRI do not show any noticeable cognitive impairments. Contrary to the characteristics of benign mesial temporal lobe epilepsy, our findings suggest that such minor structural alterations do not significantly impact the severity of epilepsy. This study emphasizes the importance of a comprehensive cognitive assessment in patients with mesial temporal lobe epilepsy, challenging previous notions about the absence of cognitive impairment in milder forms of this condition.
Ethics Approval: The conducted research was approved by the Bioethics Committee at the Medical University of Warsaw, No. KB 162/2014 of 8 July 2014.
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