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 Table of Contents  
ORIGINAL ARTICLE
Year : 2015  |  Volume : 52  |  Issue : 3  |  Page : 165-171

Assessment of precipitating factors of breakthrough seizures in epileptic patients


1 Department of Neurology, Cairo University, Cairo, Egypt
2 Clinical Neurophysiology Unit, Cairo University, Cairo, Egypt

Date of Submission24-Apr-2015
Date of Acceptance14-May-2015
Date of Web Publication13-Aug-2015

Correspondence Address:
Lamia Afifi
Clinical Neurophysiology Unit, Cairo University, Kasr Al Ainy St., Cairo 11562
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/1110-1083.162002

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  Abstract 

Background
The prevalence of breakthrough seizures is estimated to occur in 39-75.3% of epileptic patients in developing countries. Patients and physicians should be aware of the possible precipitating factors of breakthrough seizures to prevent their occurrence.
Objective
The aim of this study was to determine the precipitating factors for breakthrough seizures in patients attending Cairo University Hospital.
Methods
This cross-sectional study included 90 epileptic patients with idiopathic epilepsy receiving antiepileptic drugs (AEDs). They were divided into two groups. Group I included 55 epileptic patients with a history of recent breakthrough seizures. Group II included 35 epileptic patients who had not experienced any recent breakthrough seizures. Patients with breakthrough seizures were subjected to a thorough questionnaire addressing precipitating factors. All participants were subjected to an electroencephalogram (EEG) and the Morisky Medication Adherence Scale.
Results
Missed doses (56.4%) represented the most frequent reported precipitating factor, followed by sleep deprivation (36.4%) and psychological stress (34.5%). The patients in group I were found to have lower durations of seizure control, adherence to AEDs, and were more frequently on AED polytherapy than the participants in group II. In terms of the EEG, group I showed a higher percentage of abnormal EEGs and more frequent focal epileptiform discharges. No significant difference was found in age or sex, age at onset of epilepsy, duration of disease, and type of seizures between both groups.
Conclusion
Patients and their caregivers should be educated about these possible precipitating factors to achieve better control of epilepsy.

Keywords: breakthrough seizures, epilepsy, precipitating factors


How to cite this article:
Al-Kattan M, Afifi L, Shamloul R, Mostafa EE. Assessment of precipitating factors of breakthrough seizures in epileptic patients. Egypt J Neurol Psychiatry Neurosurg 2015;52:165-71

How to cite this URL:
Al-Kattan M, Afifi L, Shamloul R, Mostafa EE. Assessment of precipitating factors of breakthrough seizures in epileptic patients. Egypt J Neurol Psychiatry Neurosurg [serial online] 2015 [cited 2017 Jun 26];52:165-71. Available from: http://www.ejnpn.eg.net/text.asp?2015/52/3/165/162002


  Introduction Top


Epilepsy is a chronic disease affecting millions of patients worldwide, with a prevalence rate ranging from 16-51 per 100 000 population in the developed countries to 35-111 per 100 000 population in the developing countries [1]. However, it continues to be a highly stigmatized and disabling chronic condition. The limitations and restraint of activities caused by epilepsy interfere with the occupational ability and social integration of patients, and also impacts their families [2]. Moreover, it requires a long, sometimes lifelong, process of adherence to the prescriber's instructions and drug regimen [3].

The aim of treatment with antiepileptic drugs (AEDs) is to reduce the number and the severity of seizures to a minimum and preferably to none. However, up to 30% of patients with epilepsy continue to have seizures, despite attempts at treatment with a range of AEDs [4]. In patients who achieved good control on AEDs treatment, the unfortunate phenomenon of breakthrough seizures may occur. The International League against Epilepsy (ILAE) considers breakthrough seizures as seizures that occur after a seizure-free period and points out that these seizures may indicate inadequate control and hence treatment failure if poor treatment compliance and prescribed dose reductions are excluded [5]. However, there is no consensus on the definition of controlled epilepsy after which breakthrough seizures are claimed. Epilepsy was defined by Jones et al. [6] as 'well controlled' if the patient reported less than one seizure per month, whereas Sweileh et al. [7] defined epilepsy as 'well controlled' if the patient had no seizures in the last 3 months. Other studies defined controlled patients as those who had a seizure-free period for at least 6 months [3],[8]. The ILAE defines 'seizure freedom' as 'freedom from seizures for a minimum of three times the longest preintervention interseizure interval (determined from seizures occurring within the past 12 months) or 12 months, whichever is longer' [5]. Yet, they acknowledge that treatment of patients with epilepsy may lead to a clinically meaningful decrease in seizure frequency even if stopping short of seizure freedom. The prevalence of breakthrough seizures varies widely; however, it was estimated to occur in 39-75.3% of epileptic patients in developing countries [9],[10]. A single breakthrough seizure for a controlled patient has a marked impact on safety, self-esteem, social interactions, and employment [11]. It is therefore important to identify the various possible precipitating factors that may cause a breakthrough seizure once a patient is taking AEDs as this will provide valuable information to physicians involved in patient care and management of epilepsy to alert their patients of these risk factors and hopefully educate them on how to avoid them.


  Aim Top


Our study aimed to determine the precipitating factors of breakthrough seizures among known patients with epilepsy who had achieved previous seizure control for at least 6 months.


  Patients and methods Top


Patients

This study was carried out on 90 epileptic patients. All patients were recruited from the Epilepsy Clinic at Kasr Al Ainy Hospital, Cairo University. All patients were diagnosed with confirmed epilepsy in accordance with the recent definition of epilepsy by the ILEA [12]. Only patients with idiopathic epilepsy classified according to ILEA 1989 classification were included [13]. Patients were divided into two groups: group I included 55 epileptic patients who had recent breakthrough seizures defined as an epileptic seizure that occurred despite the use of AEDs in a patient who had achieved seizure control for at least the past 6 months. The control group, group II, included 35 controlled patients with idiopathic epilepsy who did not develop any recent breakthrough seizure and were matched in age and sex to the patients of group I. Patients were excluded if they showed poor history reporting or had a history suggestive of psychogenic non epileptic seizures. The experimental procedures used were approved by the local institutional ethics committee and all participants provided written or oral informed consents.

Methods

Assessment of history

All participants in this study were subjected to a thorough assessment of history, a general medical examination, and a neurological examination. A careful assessment of history of epilepsy was carried out using the Kasr El Aini Epilepsy Sheet.

Patients with breakthrough seizures were subjected to a thorough questionnaire addressing precipitating factors for breakthrough seizures. Precipitating factors were defined as those circumstances that precede the onset of an epileptic attack and are considered by both the patient and the neurologist to provide a possible explanation as to why the seizure occurred [14]. These factors included the following:

  1. One or more missed doses of AEDs before breakthrough seizures.
  2. Sleep deprivation, which could be a deficit in either the quantity or the quality of sleep versus the duration normally needed by the patient.
  3. Psychological stress, which was considered when an individual reported that the environmental emotional stress exceeded his/her adaptive psychological capacity.
  4. Flickering lights such as those that occur while watching TV or playing video games or other triggers such as flickering strobe light or sunlight.
  5. Physical and mental stress. Physical stress was defined as a transient decrease in the ability of muscles to maintain optimal physical performance because of intense physical activity. Mental stress was defined as a temporary decrease in maximal cognitive performance because of a prolonged cognitive activity. It may manifest as somnolence, lethargy, or fatigue.
  6. Concurrent fever during breakthrough seizures.
  7. Recent use of epileptogenic drugs before breakthrough seizures.
  8. Recent change of generic names of AEDs before breakthrough seizures.


Morisky Medication Adherence Scale

Adherence to AEDs in all patients was assessed using the Morisky Medication Adherence Scale (MMAS) [15]. The MMAS is a generic self-reported, medication-taking behavior scale, initially validated for hypertension, but used for a wide variety of medical conditions. The latest version of the MMAS scale is the MMAS-8, which we used in our study, and it consists of eight items with a scoring scheme of 'yes' = 0 and 'no' = 1 for the first seven items and a five-point response for the last item. The items are summed to yield a range of scores from low adherence to high adherence. A score less than 6 is considered to indicate low adherence, a score of 6-7 is considered to indicate medium adherence, and a score 8 or more is considered to indicate high adherence.

Electroencephalography

Conventional electroencephalogram (EEG) was performed for all patients to detect the presence or the type of any epileptiform discharges. All patients underwent interictal daytime EEG using the 10-20 international system for 20 min under standard conditions and using provocative techniques: photic stimulation and hyperventilation. Recordings were performed using EB Neuro Basis BE Hardware (Firenze, Italy) and Galileo Software (Firenze, Italy) for EEG data acquisition and review.

Statistical methods

Data were statistically described as mean, SD, median, minimum, maximum, frequencies (number of cases), and relative frequencies (percentages) when appropriate. For comparison of categorical data, the χ2 -test was performed. The exact test was used when the expected frequency was less than 5. A P value of less than 0.05 was considered statistically significant. All statistical calculations were carried out using statistical package for the social science (SPSS, version 21; SPSS Inc., Chicago, Illinois, USA).


  Results Top


Demographic and clinical history

The patients in group I and group II were age and sex matched, without any significant difference in age or sex (P = 0.42 and 0.32, respectively). The age at onset of epilepsy or the duration of epilepsy did not show any difference between both groups (P = 0.24 and 0.98, respectively). There was also no significant difference in the type of seizures (i.e. focal vs. generalized; P = 0.129). However, there was a significant difference between both groups in the time of the last seizure (i.e. the duration of seizure control) whether less than 1 year, 1-2 years, or more than 2 years (P < 0.001, 0.02, and <0.001, respectively). Also, the percentage of group I patients on one AED were significantly less than the percentage of group II patients on one AED (P = 0.006) [Table 1].
Table 1: Differences in history between the patients in groups I and II

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Electroencephalogram results

In group I, 33 (60%) patients had normal EEG findings, whereas 22 (40%) patients showed abnormal epileptiform discharges. In group II, 30 (85.7%) patients had normal EEG findings, whereas five (14.3%) patients had abnormal epileptiform discharges. This indicates a significant difference in the EEG findings between both groups as the finding of abnormal epileptic activity was significantly more prevalent in the patients in group I (P = 0.009). When we analyzed the type of epileptiform discharges, we found that focal epileptic activity was more common in the patients in group I (P < 0.001) [Table 2].
Table 2: Electroencephalogram fi ndings in the patients in groups I and II

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Precipitating factors

Missed doses of AEDs represented the most frequent precipitating factor among all other factors of breakthrough seizures as it was reported by 31 (56.4%) patients. The second most frequent precipitating factor was sleep deprivation, reported by 20 (36.4%) patients, followed by psychological stress, which was reported by 19 (34.5%) patients. Other precipitating factors detected in this study were flickering lights, reported by 13 (23.6%) patients, mental stress, reported by 10 (18.2%) patients, and taking epileptogenic drugs, reported by nine (16.4%) patients. Of the patients reporting epileptogenic drugs as a precipitating factor, six patients reported tramadol intake before the seizure, one patient took heroin, and the other two patients took antipsychotics; one patient took risperidone and the other patient took quetiapine. Fever was reported by seven (12.7%) patients, physical stress was reported by four (7.3%) patients, and two (3.6%) patients reported change of generic names of AEDs before breakthrough seizures [Figure 1].
Figure 1: Frequency of precipitating factors of breakthrough seizures.

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Number of precipitating factors

In group I, the absence of precipitating factors was reported by only two (3.6%) patients, 17 (30.9%) patients reported one precipitating factor, 17 (30.9%) patients reported two precipitating factors, and 19 (34.5%) patients reported more than two precipitating factors [Table 3].
Table 3: Number of precipitating factors reported by the patients in group I

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Morisky Medication Adherence Scale-8 measurement of adherence to antiepileptic drug

In group I, we found that 27 (49.1%) patients showed low adherence and 17 (30.9%) patients showed medium adherence to AEDs, whereas only 11 (20%) patients showed high adherence. In group II, we found that three (8.6%) patients showed low adherence, three (8.6%) patients showed medium adherence, whereas 29 (82.9%) patients showed high adherence to AEDs. This indicates a significant difference in adherence between both groups as the patients in group I were less adherent to AEDs than the patients in group II. They had a higher percentage of low and medium adherence, whereas the patients in group II had a higher percentage of high adherence to AEDs [Table 4].
Table 4: Adherence to antiepileptic drugs in the patients in groups I and II

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Difference in precipitating factors of breakthrough seizures in male versus female patients

On comparing male and female patients with breakthrough seizures in the study group, we found no significant difference in the frequency of precipitating factors [Table 5].
Table 5: Difference in precipitating factors between males and females in group I

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Difference in precipitating factors of breakthrough seizures between focal and generalized types of seizures

On comparing between patients with generalized seizures and those with focal seizures, there was no significant difference in the precipitating factors [Table 6].
Table 6: Difference in precipitating factors between patients with focal or generalized seizures

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  Discussion Top


To our knowledge, no studies in Egypt have been carried out to examine precipitating factors of breakthrough seizures. Therefore, we aimed to classify and analyze these factors to be able to avoid them.

On analyzing the clinical data of our cohort, we found a significant difference between both groups in the duration of seizure control, number of AEDs, and abnormal epileptic activity in EEG, whereas no difference was detected in age and sex of the patients, age at onset of epilepsy, duration of disease, or type of seizures. Patients without breakthrough seizures had a longer duration of seizure control than patients with breakthrough seizures. This is in agreement with the studies that found that a prolonged seizure-free period is associated with a reduced risk of recurrence of seizures [16]. Another significant difference was detected in the number of AEDs between both groups. Use of monotherapy was more frequent in patients without breakthrough seizures, which indicates that more AEDs were associated with higher incidence of breakthrough seizures. This may be attributed to drug-drug interactions. The pharmacokinetics of each drug influence the metabolism and subsequent effects of other drugs; for example, phenobarbital, phenytoin, and carbamazepine are potent enzyme inducers [17]. This usually results in an increase in the metabolism of the coadministered drug, followed by a decrease in its plasma concentration and its clinical efficacy. A second explanation may be the poor compliance that is commonly associated with higher doses and higher number of total daily pills taken by the patients. This agrees with previous data that found that the number of medications was an important factor affecting adherence to AEDs [18]. However, another study found that there was no significant difference in adherence between patients on monotherapy and those on polytherapy [7].

In the current study, there was a significant difference in EEG findings between both groups. The finding of epileptiform discharges was significantly higher in patients with breakthrough seizures, which suggests an association between abnormal EEG findings and breakthrough seizures. This is in agreement with previous studies that reported that abnormal EEG findings were significant predictors of poor epilepsy control [19],[20]. Similarly, our results showed that the presence of focal epileptiform discharges was higher in patients with breakthrough seizures. This is in agreement with previous data reporting that focal epileptiform discharges were associated with intractable epilepsy [21]. We found one study carried out by Shafer et al. [22] that reported that focal epileptiform activity in the initial EEG was associated with a good prognosis, perhaps because of the inclusion of a large number of patients with benign rolandic epilepsy in the study population.

On analyzing the frequency of precipitating factors related to breakthrough seizures, we found that the most frequent precipitating factor for breakthrough seizures was missed doses (56.4%). This finding agrees with that of a previous study involving 193 patients with breakthrough seizures where missed doses represented the most frequent precipitating factor, accounting for 46.6% of cases [10]. Another study found that missed doses were reported by 50% of 24 patients with breakthrough seizures aged younger than 13 years and 45.8% of 83 patients with breakthrough seizures ranging in age from 14 to 70 years, thus being the most frequent precipitating factor for breakthrough seizures in their patients [9]. This high percentage of missed doses in patients attending Kasr Al Ainy Hospital as a cause of breakthrough seizures may be attributed to the erratic supply of drugs because of the lack of financial support in addition to poor educational levels, which might hinder maintenance of proper AED use.

The second most frequent precipitating factor reported by our patients was sleep deprivation (36.4%). This is in agreement with another study by Javed et al. [9], in which sleep deprivation accounted for ∼38% of cases, becoming the second most frequent precipitating factor for breakthrough seizures. Sleep deprivation may induce seizures and epileptiform discharges in some epilepsy patients. However, seizures and some AEDs negatively affect the continuity of sleep, thus resulting in a vicious cycle [23].

The third most frequent precipitating factor was psychological stress (36.4%). Previous studies have found a strong association between stressful life events, heightened anxiety states, and seizures [24],[25]. Intake of epileptogenic drugs was reported by nine (16.4%) patients. This is not in agreement with previous studies that reported no association between epileptogenic drugs and breakthrough seizures [9],[10]. However, this may be because of the recent increase in tramadol abuse in Egypt [26].

Exposure to flickering lights was reported by 23.6% of the patients in group I. There are conflicting reports on the association of flickering light and breakthrough seizures, whereas some studies have reported no association between both, others have reported that watching TV was a precipitating factor in some patients with breakthrough seizures [9],[10],[27].

Physical stress and mental stress were reported by 7.3 and 18.2% of the patients in group I, respectively. Similarly, a previous study reported that fatigue was a precipitating factor of seizures in 15% of epileptic patients [24]. Fever because of infections was reported by seven (12.7%) of our patients with breakthrough seizures. This is similar to a previous study where fever was reported by 13% of patients to be a precipitating factor for breakthrough seizures [9]. Another study involving 1168 epileptic patients reported fever to be responsible for triggering 16.4% of seizures [25]. High-grade fever can trigger seizures in epileptic patients, especially when associated with vomiting or diarrhea, because of decreased absorption of AEDs [28].

In the present study, 3.6% of patients with breakthrough seizures reported a change in generic names of AEDs before breakthrough seizures. This low percentage may be attributed to a low number of patients who change the generic names as most patients attending Kasr Al Ainy Hospital receive their treatment from Kasr Al Ainy Hospital with almost always fixed generic names. Therefore, missing a dose was a more frequent occurrence that changing the generic type of AEDs. Changing from branded drugs to generic alternatives is usually performed on the basis of the assumption that the same efficacy can be gained at a lower price.

We found that 96.4% of patients with breakthrough seizures reported at least one precipitating factor and 65.5% of patients reported two or more precipitating factors. To our knowledge, this is the first study to assess the number of precipitating factors in breakthrough seizures. A recent study involving 89 epileptic patients found that 16 (18%) patients did not report any seizure precipitant, whereas 73 (82.2%) reported at least one specific seizure precipitant; of these, 62 (85%) patients reported two or more precipitants [29]. However, Nakken et al. [14] found that 889 of 1677 (53%) epileptic patients reported at least one seizure-precipitating factor, whereas 498 (30%) patients reported that at least two factors may have precipitated their seizure.

In terms of adherence to AEDs, patients with breakthrough seizures were less adherent to AEDs than controlled patients, which indicates an association between poor adherence to AEDs and breakthrough seizures. In our study, 80% of the patients with breakthrough seizures showed low or medium adherence to AEDs, whereas 17.1% of controlled patients showed low or medium adherence to AEDs. This is in agreement with a previous study that found that 91.9% of the participants who missed more than three AEDs doses in the week before enrollment in the study were more likely to develop breakthrough seizures [10]. Noncompliance is an important factor that needs to be addressed to reduce the incidence of breakthrough seizures. Furthermore, nonadherence may lead the physician to unnecessarily increase the prescribed dose of AEDs on the basis of the assumption that the current dose is not sufficient to control seizures. This further increases the costs of care, especially in resource-limited settings such as Egypt.

We found no significant difference in precipitating factors between males and females and between different age groups. Previous studies have reported that sex did not influence the seizure precipitants reported [10],[29]. We also found no difference in precipitating factors between patients with generalized or focal seizures. This differs to some extent from another study that found that sensitivity to sleep deprivation and flickering light was greater in patients with generalized seizures than in those with partial seizures, although both patients seemed to be equally sensitive to emotional stress and tiredness [14]. This difference from our results may be attributed to differences in the populations involved as their study included epileptic patients from several epilepsy centers with different types of epilepsy with and without known etiology, whereas in our study, we included patients with only idiopathic epilepsy, with fewer patients.

Although many precipitating factors have been described in the literature, sometimes more than one factor can coact, leading to a complex relationship between precipitating factors and the occurrence of seizures; for instance, emotional stress may further lead to excessive alcohol drinking, noncompliance, and sleep deprivation. Seizure-precipitating factors should therefore be taken into account in patient education and in tailoring of their treatment regimens. For instance, psychological interventions may be useful in control of stress-induced seizures [29]. We recommend carrying out similar studies with a larger sample size and using AED serum levels and toxicology screens to provide additional objective data as such studies have so far relied on self-reporting by the patients. The clinical relevance of knowing what precipitates seizures cannot be overemphasized.

Acknowledgements

Nil.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
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    Figures

  [Figure 1]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]


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