Epilepsy and education: A case-control analysis of the impact of an intensive epilepsy training program on undergraduate medical students

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Introduction
Epilepsy is one of the most common and serious chronic neurological conditions affecting more than 70 million people worldwide [2,3].However, it is estimated that approximately 80 % of people with epilepsy live in developing countries, representing a major public health problem [4].Epilepsy affects the social, economic, physical, and mental health aspects of peopleś lives, which is reflected in prevalent stigma and discrimination in the social environment generalized around the world [5].The prevalence of epilepsy in Mexico is estimated between 10.8 and 20 cases per thousand inhabitants [6].
The lack of qualified personnel such as primary care physicians and specialized clinicians in neurology and epilepsy, the cost of treatment, the unavailability of drugs, cultural beliefs, the use of traditional medicine, and the distance to a health center are the main causes of treatment failure in epilepsy in developing countries [7][8][9].Education is an integral part of the multidisciplinary management of epilepsy and the means whereby health professionals, patients, families, and the public at large need to be aware of epilepsy [7,10].Academic training for health professionals from different disciplines and levels of education, Abbreviations: TUMSs, Trained undergraduate medical students; KAP, Knowledge Attitudes and Practices; ASM, Antiseizure medication; ILAE, International League Against Epilepsy.including medical undergraduate students, is paramount and is part of the mission of the ILAE to understand, diagnose, and treat persons with epilepsy in several settings [11].Greater knowledge of medical undergraduate students will eventually lead, after graduation, to improve the quality of medical care provided to persons with epilepsy in the community.
The cornerstone of effective diagnosis and treatment is education.Developing an epilepsy educational curriculum serves as a starting point for creating training programs aimed at improving epilepsy awareness and knowledge among medical students.According to the assessed students in this study, the average duration for compulsory instruction on epilepsy in Mexican universities is approximately 2 h.On the other hand, the practical hours vary depending on the cases observed in the outpatient clinic and the ones hospitalized.The interest of the training physician and the students in the topic of epilepsy plays an essential role when obtaining practical skills.Therefore, a proper educational plan should be established to teach the most essential knowledge to medical undergraduate students to prepare them to approach and manage people with epilepsy in the best way.
The purpose of the study was to assess the level of knowledge, attitudes and practical skills in medical undergraduate students who attended a 6-week Intensive Clinical and Research Program in Epilepsy in a neurological center in Mexico City compared with medical students without any specific training using the KAP survey.We hypothesized that the medical undergraduate students submitted to intensive training would display better performance in theoretical and practical skills, and positive attitudes toward people with epilepsy.

Study design
The research is a prospective, case-control study.The cases of TUMS were paired with medical students without any epilepsy training with the same age, university of origin, academic year, and compulsory hours for learning about epilepsy.The sole distinction between the groups lies in the educational intervention.The evaluation was performed based on the baseline knowledge, attitudes, and practices (KAP) survey model related to epilepsy among medical undergraduate students.

Study population
Our population consisted of Mexican medical undergraduates who underwent training from 2020 to 2023, matched with peers of the same age, university, academic year, and required hours for studying epilepsy who did not receive such training.
Medical students from various parts of Mexico, spanning the entire six-year medical bachelor program, had the opportunity to undergo epilepsy training.Due to constrained educational resources, five students were chosen in the initial two years and six in the subsequent two editions.The selection of participating students was based on their demonstrated interest and enthusiasm for neurology and research during a brief interview.
The students who participate in the study were from the Meritorious Autonomous University of Puebla (Benemérita Universidad Autónoma de Puebla; BUAP), the National Autonomous University of Mexico (Universidad Nacional Autónoma de México; UNAM), the National Polytechnic Institute (Instituto Politécnico Nacional; IPN), the Autonomous University of Chiapas (Universidad Autónoma de Chiapas; UNACH), and the Autonomous University of the Estate of Mexico (Universidad Autónoma del Estado de México; UAEM).
After the completion of the intensive program, 22 medical undergraduate students who were members of the intensive program were evaluated with the questionnaire KAP on epilepsy-related topics.For the control group, the KAP questionnaire was administered to other 22 undergraduate medical students.

Data collection and data management
For the data collection, an online survey form was created in Google Forms.Before students and their peers complete the questionnaire, we provided detailed information about the research objectives, data confidentiality measures, assurance of anonymity and finally requested their consent to participate in the study.The universities of the participants were also informed about the acceptance of the undergraduate students, the planned activities, and the evaluation of the students after the intensive training.We clarified the data protection and management in detail to each university.They were also informed that the information obtained from the survey can be used in research activities.

Structure of the program
The program consisted of a 6-week training divided into a structure of two main items: knowledge, attitudes and practice; see Table 1 The educational team was composed by 5 epileptologist, and 1 clinical researcher.Each student was paired with an epileptologist.Health professionals from pathology, neurosurgery and nursing departments have also contribute to the intensive training.
Concerning the practical applications of procedures and protocols related to epilepsy, students were introduced to strategies for managing individuals experiencing seizures.They were acquainted with hospital guidelines and participated in simulations to guarantee their proficiency in responding appropriately.

Statistical analysis
Statistical analyses were carried out using SPSS software (IBM, version 25.0)To identify statistical distinctions among the correct answers between groups, we employed the Fisher exact test for binary categorical variables and the χ 2 test for categorical variables with more than two levels.The variables examined encompassed the related answers from 25 questions, in which the practical skills and knowledge were assessed.In the context of descriptive statistics, dichotomous and ordinal variables were represented by indicating the number of subjects and their corresponding percentages.Continuous variables were displayed using the average and standard deviation (SD).A significance level of 0.05 was utilized.

Demographics
Table 2 shows the characteristics of the control and trained groups.Both arms displayed similar age, academic year, and compulsory hours for learning about epilepsy.

Assessment of theoretical knowledge
Regarding mastering basic terms, TUMSs showed a stronger understanding of distinguishing between seizures and epilepsy than the control group (100 and 82 %; p = 0.0036).In addition, TUMSs related CNS tumors as one of the main causes of epilepsy compared to the control group (CG) (90 and 9 %; p = 0.001).Conversely, the control group recognized persistent avitaminosis as one of the leading causes of epilepsy in comparison to the TUMS group (36 and 9 %, p = 0.0034).Furthermore, hippocampal sclerosis was more supported in the TUMS group as a structural entity and a main cause of epilepsy than in the control arm (91 and 46 %, p = 0.001) [Table 3].
Concerning the paraclinical studies used in epilepsy diagnosis, MRI was the most chosen imaging technique in the TUMS group (91 and 64 %, p = 0.031).Meanwhile, the cerebrospinal fluid analysis was the most selected option in the control arm (36 and 0 %; p = 0.002).Moreover, TUMS group requested neuroimaging when a structural origin of the seizures was suspected more often compared to the control group, coinciding with the ILAE guidelines (73 and %, p = 0.025) [Table 3].

Assessment of attitude perspectives
TUMSs considered that individuals with epilepsy face limited   4].

Assessment of practical skills
Among the main goals to achieve in people with epilepsy, TUMS group considered the importance of allowing them to maintain a normal occupation more relevant compared to the control group (86 and 55 %; p = 0.021).Similarly, both groups (91 % and 91 %; p = 0.697) expressed that minimizing the influence of seizures on the quality of life is the primary objective to attain for individuals with epilepsy.Of the treatment options, the TUMS group frequently mentioned electrical stimulation as a therapeutic option for epilepsy than the control arm (91 and 36 %; p = 0.001) [Table 5].
On the subject of ASM treatment, both the TUMS and control groups had a similar number of medical students who were in charge of the treatment of persons with epilepsy.However, more undergraduate medical students of the trained group measured the levels of ASMs after modifying the treatment scheme compared to the control group (Always 18 and 0 %, frequently 23 % and 0 %; p = 0.004).When a patient remains without seizures for at least 2 years, all TUMSs suggested stopping the ASM therapy, while just 77 % of the medical students in the control group recommended this option (p = 0.024).In response to the question of whether epilepsy can be cured with ASMs, all TUMSs answered that epilepsy can be controlled but cannot be cured (100 % and 82 %; p = 0.044).For the management of epilepsy during pregnancy, all TUMSs have recommended to continue with the ASM treatment compared to % of the medical students in the control group (p = 0.004) [Table 5].
Finally, providing seizure first aid was evaluated.The control group was more focused on moving objects away from the person (73 and %; p = 0.015) and putting an object in his mouth (18 an 0 %; p = 0036), while the TUMS group considered more relevant moving the person to a more secure place (100 and 82 %; p = 0.036) [Table 5].

Discussion
Our study provides evidence of the effectiveness of intensive training, not only in enhancing understanding of fundamental epilepsy concepts but also in improving the proficiency in the management and follow-up of patients with epilepsy.Based on the experience of neurological experts, an intensive clinical training program was founded to approach the most common gaps, teaching the most essential knowledge to undergraduate students who will become general practitioners.
Numerous studies have explored the knowledge, attitudes, and practical skills of medical students regarding epilepsy without any educational intervention, both in developed and developing countries like ours [1,[13][14][15][17][18][19]21,[23][24][25][26][27], with findings indicating a lack of knowledge of epilepsy.Contrastingly, only in four research studies educational approaches were applied.We observe the significance of the duration of the educational intervention and the outcomes post-training.Longer training durations were associated with more favorable results [16,17,20,22].Keeping this in mind, we have implemented a 6-week training program in epilepsy for undergraduate students with promising results.Therefore, we encourage more hospitals and universities to establish training programs for students based on our model.In the case of tailoring the training program, we recommend implementing the KAP instrument to identify weaknesses in the population of students.

Table 4
Results of the attitude in the epilepsy section in the trained and control groups.

Positive impact of the intensive training on the knowledge of the trained students
Beyond knowing the difference between epilepsy and seizures, the relevance lies in the difference between etiologies and further management.The distinction between seizures and epilepsy drives the use of ASMs or control of the subjacent disease with neurological manifestations [39,40].
To recognize tumors as one of the main causes of epilepsy is essential for both clinicians related and non-related to neurological disease, because brain tumors are the etiology behind epilepsy in more than 80 %, while around 20 % of the epilepsy cases have a relationship with metastasis to CNS structures [41,42].Therefore, epilepsy is the recurrent neurological manifestation that can give clinicians the hint of facing any kind of tumor that can be early approached, while the related epilepsy can be better controlled.Conversely, avitaminosis caused confusion among the control group, and we postulate that such confusion can be associated with vitamin B and folates and further vitaminic deficits and chronic neurological disorders, such as Alzheimer's disease, Parkinsonś disease, and depression among others [43].Likewise, hippocampal sclerosis is an important cause of refractory epilepsy, and the term and the potential clinical implications is taught to undergraduate students as pathology with a surgical solution.After offering surgical interventions for patients with hippocampal sclerosis, approximately 80 % of the patients experience no seizures even without ASMs, for up to 23 years post-surgery [44,45].
About the neuroimaging tools, MRI is a primary paraclinical study that provides information about a suspected structural origin of seizures or epileptogenic brain abnormality and its surrounding anatomy.Among the epileptogenic pathologies, some of them can be surgically treated and first approached by MRI [46,47].Experts consider MRI essential for guiding the diagnosis, treatment, and prognosis of patients with epilepsy, irrespective of lesional or non-lesional etiologies-a concept well grasped by the TUMS.Regarding the CSF analysis, it was controversial, but it is not considered a basic paraclinical study for epilepsy diagnosis.However, inflammatory entities can cause seizures, and the CSF analysis is the standard method to determine the main cause of the inflammatory process [48,49].
Regarding when to request a neuroimaging study, an important point stands out, since it is crucial to consider the debate surrounding its performance, even contemplating the possibility of performing it routinely.However, we emphasize that, in the first instance, the request for these studies should be based on the suspicion of a structural abnormality.This is relevant because it is essential to recognize that many of these studies are not available in our hospitals at the primary care level, where most undergraduate students gain experience.In this context, the expertise and specialization needed to interpret these studies may not be readily available.Therefore, for our TUMS, the primary focus should be on developing the ability to recognize and appropriately refer patients, taking into account these limitations.When a more specialized evaluation is needed, consider the option of referring cases to a higher level of health care.

Slight influence of the intensive training on the attitude of the trained students
In the attitude assessment, the difference between the outputs from the control group and the TUMS was reduced.The education level might influence the attitude toward epilepsy [1,13].It was observed that educated participants were more inclined to express positive feelings toward individuals with epilepsy in comparison to those who were not literate, demonstrating traits such as tolerance, kindness, and sympathy.Moreover, literate people believe that people with epilepsy can succeed academically, can perform recreational activities, can marry, and have children [14].In medical fields, the attitudes towards people with epilepsy vary based on the academic year, with students in clinical years getting better results compared to the ones in the preclinical phases [14,19].In our study, both clinical and preclinical students obtained similar results in this regard.There is a debate surrounding the attitudes of students from various disciplines towards epilepsy.Mewes and colleagues noted minor distinctions in the attitudes of students from diverse fields toward individuals with epilepsy [50].In contrast, Hijazeen et al. found that humanities students exhibited more unfavorable attitudes compared to their homologous in the science faculty [18].Additional research is needed to address this dilemma.
Based on the TUMSs perspective (86 %), individuals with epilepsy encounter restricted opportunities to sustain their social life and employment.The results contrast with the ones reported in past works, in which undergraduate medical and other health science students, as well as general practitioners, expressed that people with epilepsy can have social inclusion and perform any job even in the most demanding professions [14,17,23,26].The possible explanation is related to workplace accidents as reported by more than half of TUMSs (68 %), which could be considered when hiring a person with epilepsy.Other factors such as beliefs and preconceptions can negatively influence the attitude toward epilepsy [13,15,21,25].
As a new discussion topic, TUMSs (73 %) highlighted that facing epilepsy in Mexico represents a considerable risk due to the difficulties linked to diagnosis.Moreover, TUMSs (73 %) highlighted the considerable challenge that epilepsy poses for general practitioners in Mexico when it comes to diagnosis and subsequent monitoring.Delays in receiving a diagnosis and challenges in subsequent monitoring are evident in both developing countries and nations with sufficient access to medical care [51].There is a lack of information from other studies about both topics, but the perception of TUMSs is clear in a developing country such as Mexico, remaining open to be studied in developed nations.

Beneficial effect of the intensive training on the practical skills of the trained students
Aside from the practical skills, the establishment of main goals to achieve in the management of patients with epilepsy is one of the tasks conducted by trained healthcare providers.Epilepsy confers a high rate of unemployment [52].Therefore, social awareness about the capabilities of people with epilepsy to perform work tasks in standard workplaces is taught to trained students and further disseminated in society, in specific workers and employers.
As expected, the trained students had more knowledge about electric stimulator devices for epilepsy such as the vagus nerve stimulation (VNS), deep brain stimulation of the anterior nucleus of the thalamus and responsive neurostimulation (RNS).However, the device they recognized the most is the transcranial Direct Current Stimulation (tDCS), which is an experimental treatment of epilepsy with a successful application in patients with temporal lobe epilepsy and hippocampal sclerosis [53].We also documented the reduction in the seizure duration during the application of tDCS [54].The results are promising but further studies should be replicated in other neurological centers to corroborate the efficacy of tDCS.Regarding the trained students, they were engaged proactively in tDCS sessions under the supervision of experienced clinicians, enhancing the learning experience in a more meaningful manner.
From the trained students who treat patients with epilepsy today (10, 46 %), nine of them always or frequently determine serum levels of the ASMs when adjusting the treatment, compared to students in the control group, who rarely (2, 9 %) conduct such blood test.The estimation of ASMs in blood helps clinicians to corroborate the effectiveness of the treatment according to medication doses to avoid adverse effects at high doses.It can also be critical to prove a possible non-compliance and monitor the blood level of ASMs in scenarios where the pharmacokinetic is compromised, including fast metabolizers, pregnancy, hepatic or renal dysfunction, children, and elderly patients [55,56].The main objective is to optimize the ASM treatment for each patient.In cases of refractory epilepsy, TUMSs show a tendency to consult an epilepsy center compared to the control group (55 % and 27 %; p = 0.066).To promote the reference and consultation of epilepsy centers, we plan to develop new protocols in the matter, wherein TUMSs will participate actively to gather the substantial knowledge.
During medical counseling, clinicians should be clear that the epilepsy is controlled under ASMs treatment but not cured.This information was reported by 100 % of TUMSs in the KAP survey.According to the World Health Organization (WHO), up to 70 % of epilepsy patients can achieve freedom from seizures with the proper use of ASMs.We shared these facts with trained students so that they can explain to patients with epilepsy the relevance of ASMs in their lives and encourage them to adhere more diligently to pharmacological treatment.Furthermore, we recommend the trained students to gradually reduce the ASMs until it is no longer taken in patients with at least 2 years without experiencing seizures.The idea is to avoid adverse effects in patients for whom the administration of ASMs is no longer necessary.However, the decision should be made based on the specific case of the patients [57][58][59].The knowledge about stopping ASMs in individuals with seizure remission was so clear for TUMSs that all of them could correctly answered where and when to do so.
In cases of epilepsy during pregnancy, the trained students learned that it is recommended to continue with the ASM treatment, being 100 % of them who conveyed this fact.Lamotrigine and Levetiracetam stand out as the optimal choices for continuing pharmacological treatment without posing fetal risks of malformations and minimizing maternal risks associated with uncontrolled seizures [60,61].
Seizure first aid is one of the special topics we reinforced in our intensive training to teach the trained students how to react when a person experiences a seizure.All TUMSs (22, 100 %) understood that a person suffering a seizure should be removed from a dangerous place.Our concern is that the majority of the population refers to incorrect interventions that would rather deteriorate the current status of the person with a seizure [62].An example of this is the control group's response of placing an object in the person's mouth (4, 18 %).Even healthcare providers find themselves unprepared to act when they encounter a person experiencing seizures.Fortunately, the training in first aid for seizures encourages them to confront such situations, improving their performance after receiving guidance from experts [63].

Relevance of the intensive training in medical undergraduate students
In Mexico, the prevalence of epilepsy is estimated between 10.8 and 20 cases per thousand inhabitants [6], cases that newly graduated physicians will be responsible for.Their role in the early diagnosis of epilepsy and further patient reference is crucial since they are the first contact or primary care physician.Some other duties of general practitioners, general neurologists, and epilepsy specialists in the management of patients with epilepsy are listed in Fig. 1, a modified figure from Hutchinson and collaborators [64].
Unfortunately, the Mexican Ministry of Health reported a shortage in general neurologists, having 1 per 100,000 inhabitants nationwide, registering 3 neurologists per million inhabitants in 5 Mexican states.The lack of specialists in neurology and epilepsy forces primary care physicians to take charge of their duties [Fig.1].Hence, there is an urgency to implement intensive training for primary care physicians.The significant risk associated with the absence of epilepsy training is the potential for misdiagnosis and delayed treatment of patients with epilepsy.

Limitations of the study
The main limitation of the study is the size of the sample.To ensure a fully immersive educational setting, the calculation of potential participants for the rigorous training relied on the available epileptologists to supervise students throughout all planned activities.Additionally, the clinical institution imposes limitations on the number of students permitted to partake in the intensive training, attributed to spatial constraints within the hospital facilities.To overcome this limitation, a larger sample size could be explored in the future, allowing for the inclusion of subsequent generations of undergraduate students in the intensive training.
The level of interest in the subject of "epilepsy" also contributes to the learning process, motivating TUMSs to dedicate substantial effort to studying epilepsy and exploring related subjects more than students with different academic interests.To mitigate this influence, one strategy is to randomly assign students to intensive training, regardless of their academic preferences, and assess their knowledge, attitudes, and practical skills after the course.

Conclusions
In conclusion, our case-control study successfully compared the knowledge and practical skills of medical undergraduate students who underwent a specialized 6-week training program in epilepsy with their counterparts who received mandatory neurology classes but lacked specific epilepsy training.The trained students demonstrated notable improvements in their understanding of fundamental epilepsy concepts, causes, and essential paraclinical studies.Moreover, trained medical undergraduate students who treat daily patients with epilepsy exhibited enhanced proficiency in adjusting and monitoring treatments, especially in unique cases such as those related to pregnancy.Importantly, the trained students also displayed a greater knowledge base in seizures first aid.Overall, these findings affirm that the intensive education program significantly contributes to the enhancement of knowledge, attitudes and practical skills among undergraduate students in the field of epilepsy care.The primary constraint in our research lies in the size of the sample, and it is advisable to investigate larger groups for validation of the present findings.However, the output here presented exhibits that the implementation of intensive epilepsy programs can be beneficial for countries with a shortage of neurology specialists, as primary care physicians could take on the management and follow-up of patients with epilepsy.

Table 1
. This program serves as a foundational model applied annually to students, following a continuous education approach by CAMELICE (Mexican Chapter of the International League Against Epilepsy).The program was meticulously prepared by experts in epilepsy associated with the ILAE Mexico program.It is emphasized that the program was tailored to address identified needs and includes auxiliary tools integrated into the academic training of undergraduate physicians.The sources utilized for Structure of the Intensive Epilepsy Training Program.

Table 2
Demographic features of the trained and control groups.

Table 3
Results of the knowledge in the epilepsy section in the trained and control groups. of maintaining their social life and employment compared to the opinion of the control group (86 and 27 %; p = 0.001).According to TUMS, people with epilepsy are more susceptible to workplace accidents in the job environment (68 and 27 %; p = 0.006).TUMSs pointed out that experiencing epilepsy in this country poses a significant risk due to the challenges associated with diagnosis (73 and 23 %; p = 0.004).Additionally, TUMSs emphasized that epilepsy is a particularly challenging condition for general practitioners in Mexico to diagnose and follow-up (73 and 36 %; p = 0.018) [Table + Pearson's chi-square test.* Statistically significant.R. Diaz-Peregrino et al. prospects

Table 5
Results of the medical practice in epilepsy section in the trained and control groups.