Al-Azhar Assiut Medical Journal

ORIGINAL ARTICLE
Year
: 2016  |  Volume : 14  |  Issue : 3  |  Page : 140--145

The predictive value of electroencephalography in recurrence of the first-ever unprovoked idiopathic seizure


Nabil Abd Al Hakim Metwally, Mahmod Mohamad Hasan, Yaser Hamed Mostafa 
 Neuro-psychiatry Department, Alazahr University Hospitals, Assiut, Egypt

Correspondence Address:
Mahmod Mohamad Hasan
Neuro-psychiatry Department, Alazahr University Hospitals, Assiut
Egypt

Abstract

Aim of the study We aimed to study the role of electroencephalography (EEG) and its predictive value for recurrence after the first-ever seizure. Patients and methods Patients who presented with first idiopathic seizure attack were included in this prospective study. The study group included 70 patients (39 male and 31 female). Their ages ranged from 1 to 58 years. All patients included were subjected to history taking and full analysis of the seizure, full neurological examination, routine laboratory tests, neuroimaging, and EEG evaluation, and then all patients were interviewed monthly for 3 successive months. Results Sixteen patients (23%) had focal seizures and 54 patients (77%) had generalized seizure. Nocturnal seizures were found in 45.7% of patients, whereas diurnal seizures were found in 54.3% patients. Aura was recorded in 17% of cases, whereas postictal state (confusion, headache, muscle ache, and Todd’s paralysis) occurred in 60% of cases. Past history of febrile seizures was present in 17% of cases, family history of epilepsy was positive in 10% of cases, and 31.4% of cases had positive consanguinity. Abnormal EEG was found in 54.3% of patients [31.4% of patients had generalized epileptiform discharge, 15.7% of patients had focal epileptiform discharge with or without secondary generalization, and 7.2% of patients had no specific changes (focal or generalized slowness)] and lastly normal EEG was found in 45.7% of patients. After 3 months of follow-up, 37 patients (52.9%) had recurrence of seizure: 75.6% of patients had generalized seizures and 24.4% of patients had focal seizures. The percent of recurrence among patients with abnormal EEG was 70.3% and that among those with normal EEG was 29.7%. As regards EEG findings, there were a significant correlation between abnormal EEG and generalized epileptiform discharge and recurrence of seizure. Conclusion EEG, especially during the first 48 h after seizure, had a prognostic value for recurrence of seizure.



How to cite this article:
Metwally NA, Hasan MM, Mostafa YH. The predictive value of electroencephalography in recurrence of the first-ever unprovoked idiopathic seizure.Al-Azhar Assiut Med J 2016;14:140-145


How to cite this URL:
Metwally NA, Hasan MM, Mostafa YH. The predictive value of electroencephalography in recurrence of the first-ever unprovoked idiopathic seizure. Al-Azhar Assiut Med J [serial online] 2016 [cited 2020 Jul 15 ];14:140-145
Available from: http://www.azmj.eg.net/text.asp?2016/14/3/140/200153


Full Text

 Introduction



The term ‘seizure’ refers to the transient clinical manifestation of an episodic, abnormal, excessive, and hypersynchronous discharge of a population of epileptic cortical neurons. For a particular patient, the seizure tends to be stereotyped, although it may take many forms (mixed seizure types) in others. The form of seizures in epilepsy could be conceptualized according to how it is experienced by the patient (as a motor, somatosensory, autonomic, or psychic manifestation with or without impaired level of consciousness) or, more conveniently, on physiological grounds, as either focal or generalized, in relation to how seizure activity originates within the brain [1]. According to the International League Against Epilepsy (ILAE), a first unprovoked seizure is a seizure occurring in a person over 1 month of age with no prior history of unprovoked seizures [2]. About 1% of people worldwide (65 million) have epilepsy and nearly 80% of cases occur in developing countries. About 5–10% of all people will have an unprovoked seizure by the age of 80, and the chance of experiencing a second seizure is between 40 and 50% [3]. The risk for recurrence of first unprovoked seizure is 30–50%. Even one seizure is a traumatic physical and psychological event that poses difficult diagnostic and treatment questions, and has major social consequences. Recurrent seizures pose even more serious and costly problems [4]. There are two factors that are consistently associated with an increased risk for seizure recurrence in both children and adults: an abnormal electroencephalography (EEG) (particularly if the abnormality is epileptiform), and a symptomatic cause or abnormal neurological examination. The two factors may have a somewhat additive effect in that patients with both a symptomatic cause and an abnormal EEG appear to have an even higher risk than those with only one of those factors [5]. The estimated probability of seizure recurrence after a first seizure during childhood increases from 27 to 42% if the EEG is normal and increases from 60 to 71% if epileptiform abnormalities are seen. However, in adults with epileptiform EEG abnormalities the risk for recurrence is 49.5%, compared with 27.4% in individuals whose EEGs are completely normal [6]. EEG is usually a necessary diagnostic tool for the evaluation of seizures. Clinicians use EEG especially to answer the following questions: Is the paroxysmal event epilepsy versus nonepileptic attacks (syncope, nonepileptic psychogenic seizure, etc.), what type of epilepsy is it (etiology, seizure type, and syndrome), what is the prognosis (especially after a single seizure, or after surgery), and what is the effect of antiepileptic treatment (especially in status epilepticus, could they be stopped with treatment) [7]. EEG is used as one of the several variables and can identify children with very high and very low recurrence risks. It influences the decision to perform subsequent neuroimaging studies and may influence counseling on management of the child. As such, it is recommended that an EEG be performed after the first nonfebrile seizure in sleeping children [4].

 Patients and methods



The patients who presented with first idiopathic unprovoked seizure were included in the study. The study group included 70 patients (39 male and 31 female). Their ages ranged from 1 to 58 years. They attended the emergency department or outpatient clinic of Neuropsychiatry Department of Al-Azhar University Hospitals (Assiut and Cairo) during the period from 1 October 2015 to the end of May 2016. This study has been approved by the ethical committee of the Faculty of Medicine, Al-Azhar University. Moreover, written consent was obtained from all patients or his/her parents for participation in the study and the objectives of the study were briefly and clearly described orally as well before obtaining the consent and participation in the study. Any patient with recurrent seizures, symptomatic epilepsy (including stroke, head trauma, metabolic disturbances, etc.), delayed motor and mental development, drug and alcohol abuse, conditions mimicking epilepsy (psychogenic nonepileptic fits, vasovagal attacks, syncope, transient ischemic attacks, sleep disorders, panic attacks, or behavioral events), or abnormal neuroimaging computed tomography and/or MRI brain was excluded from the study. All patients included in the study were subjected to a complete history taking as regards a detailed history of seizure, other neurological manifestations (increased intra cranial pressure (ICP) manifestations, cranial nerves, motor, sensory systems, and sphincter disturbances), reviewing the manifestations of other system affection, past history of prior seizures, symptoms suggestive of seizures, febrile seizures, chronic disease, and family history including positive family history of epilepsy and consanguinity. All patients were generally examined for vital signs, extremities, cardiovascular, hepatic, renal, respiratory system, and skin. Neurological examination was carried out, including mental state, cranial nerves, motor, sensory systems, cerebellum, gait, back, spine, bone, and meningeal irritation signs. Laboratory investigations included complete blood count, kidney function tests, liver function tests, serum electrolytes (Ca, Na, and K), random blood sugar, neuroimaging computed tomography scan and/or MRI brain. As regards the EEG, all patients were referred to the neurophysiology unit and EEG was recorded within 48 h from the seizure onset. EEGs were recorded on 64-channel machine with both referential and bipolar recordings using the international 10–20 electrode placement system. Time of recording was not less than 20 min for all patients. Patients subjected to EEG recording were awake (some patients fell asleep during examination) and were instructed to close both eyes with complete physical and mental relaxation; however, pediatric patients were induced sleep at recording using oral chloral hydrate at a dose of 50–100 mg/kg [8]. Activation procedures such as hyperventilation and photic stimulation were used in most of the patients to enhance the chance of recording the epileptic activity. Hyperventilation was performed for a minimum of 3 min with continued recording for at least 1 min after cessation of overbreathing [9]. Hyperventilation cannot be performed in the pediatric patients. Intermittent photic stimulation was used in the following sequence at a distance of 30 cm from the patient’s face 1, 2, 3, 4, 6, 8, 10, 12, 14, 16, 18, and 20 Hz [10]. Patients were monitored for artifacts by the trained experts. In addition, additional electrodes for monitoring eye movement, ECG, and muscle activity were used [11]. EEG changes were classified as normal EEG (N), generalized epileptiform discharge (GED), focal epileptiform discharge with or without secondary generalization and nonspecific changes (focal or generalized slowness) [12]. After that, all patients included in the study were interviewed monthly for 3 months through clinical visits for recurrence. Ethical consideration: (a) Risk–benefit assessment: There was no risk during application of the research. (b) Confidentiality was maintained during the research. Informed oral and written consent was taken from patients or their close relatives for their approval to participate in this study.

 Results



The study was carried out on 70 patients with idiopathic single seizure [39 male (55.7%) and 31 female (44.3%)]. The mean age of the studied patients was 17.5±17 years and ranged from 1 to 58 years. On the basis of International League Against Epilepsy (2010) of epileptic seizures, 16 patients (23%) had focal (partial) seizures and 54 patients had (77%) generalized seizure ([Table 1]).{Table 1}

Nocturnal seizures were found in 45.7% of patients, whereas diurnal seizures were found in 54.3%. Aura was recorded in 17% of cases, whereas postictal state (confusion, headache, muscle ache, and Todd’s paralysis) occurred in 60%. Past history of febrile seizures was present in 17%, family history of epilepsy was positive in 10% of cases, and 31.4% of cases had positive consanguinity ([Table 1] and [Table 2], [Figure 1]).{Table 2}{Figure 1}

According to EEG findings, abnormal EEG was found in 54.3% of patients [31.4% of patients had GED, 15.7% of patients had focal epileptiform discharge with or without secondary generalization, 7.2% of patients had nonspecific changes (focal or generalized slowness)] and lastly normal EEG was found in 45.7% of patients ([Table 3] and [Figure 2]). After 3 months of follow-up, 37 patients (52.86%) had recurrence of seizure ([Table 3] and [Table 4]).{Table 3}{Figure 2}{Table 4}

As regards age, sex, time of seizure (diurnal or nocturnal), aura, postictal state, family history of epilepsy, positive consanguinity, past history of febrile seizure, and type of seizure, no significant correlation was found between them and recurrence of seizure ([Table 5] and [Table 6]).{Table 5}{Table 6}

In all, 75.6% of patients had generalized seizures and 24.4% of patients had focal seizures ([Table 6]).

As regards EEG finding, there was a significant correlation between abnormal EEG and GED and recurrence of seizure ([Table 7]).{Table 7}

 Discussion



In the present study, 70 patients who presented with idiopathic unprovoked first seizure attack were included in the study. After 3 months of follow-up, 52.8% of patients had recurrence of seizure. The results of the study were slightly lower compared with the results reported by Martinovic and Nebojsa [13], who reported that the second seizure occurred in 69.2% of cases, most commonly during the first 3 months after the first seizure in 70.37% of cases, and Pairoj [12], who reported that the recurrence rate was 68% after first seizure; most of them (50%) occurred within 4 months. Arthur et al. [14] reported that the recurrence rate of unprovoked seizure before 9 months was 58.0%, that before 18 months was 62.0%, and that before 27 months was 66.0%. However, Hirtz et al. [15], Elwes et al. [16], and Hart et al. [17] reported 81, 69, and 71% recurrence rate, respectively. The results of the study were higher than the results reported by Scotoni et al. [18], who reported that the recurrence was 34%, and the mean time for recurrence was 12 months, and Anang and José [19], who reported that the seizure recurrence was 25.5% after a follow-up of at least 12 months.

As regards age and sex, the results of the study showed that the mean age for patients with recurrence was slightly lower than that in those with nonrecurrence, and the incidence of recurrence was slightly higher among female than among male patients without a significant difference. These results are in agreement with those of Pairoj [12] in Thailand, Scotoni et al. [18] in Brazil, and Davis [20], who reported that age and sex were not significant risk factors for seizure recurrence. Bessisso et al. [21] reported that young age is a risk factor for seizure recurrence and that the rate of recurrence at 1 year for patients who were 15 years and younger was 70%, as compared with 63% for those between 16 and 39 years and 55% for those between 40 and 59 years.

As regards family history of epilepsy, the results of the study showed that the incidence of recurrence was slightly higher among patients with positive family history of epilepsy, without a significant difference. These results are in agreement with those of Pairoj [12] in Thailand and Scotoni et al. [18] in Brazil, who reported that positive family history of epilepsy was not a significant risk factor for seizure recurrence. Our results are in disagreement with those of Hauser et al. [22], Bessisso et al. [21], and Radhakrishnan et al. [28], who reported that seizure recurrence rate was significantly increased among those with a positive family of epilepsy. This difference in the results may be attributed to the difference in the definition of positive family history and longer follow-up duration.

In the present study, there was a nonsignificant correlation between type of seizure, presence of aura, presence of postictal symptoms, and past history of febrile seizure and recurrence of seizure. These results are in agreement with those of Scotoni et al. [18] in Brazil, who reported that the seizure type, presence of aura, presence of postictal symptoms and past history of febrile seizure were nonsignificant risk factors for seizure recurrence. This is in disagreement with the findings of Camfield et al. [23] and Stroink et al. [24], who reported that partial seizures, abnormal neurological examination, and mental retardation were risk factors for seizure recurrence. Shinnar and Berg [25] showed that idiopathic partial seizures with normal EEG were not associated with a significant increase in risk for recurrence. An increased risk associated with partial seizures cannot be definitely excluded, particularly in individuals with a symptomatic first seizure ([22],[26]).

In the present study, the recurrence of seizures was slightly higher in nocturnal seizure than in diurnal seizure, without a significant difference. These results are in agreement with those of Scotoni et al. [18], who reported that the recurrence of nocturnal seizure occurred in 48% of cases, whereas recurrence of diurnal seizures occurred in 30% of cases, without a statistically significant difference. In the present study, the recurrence of seizures occurred among 57% of patients with past history of febrile seizures, without a statistically significant difference. These results are in agreement with those of Anang and José [19], who reported that the past history of febrile seizure was a nonsignificant risk for recurrence.

In the present study, EEG abnormality was recorded in 54.3% of patients; of them, 47% had epileptiform focal or generalized (spike and sharp wave) and 7.2% had nonepileptiform (focal and generalized slowness). 31.4% of patients had GED, 15.7% had focal epileptiform discharge, and 7% had focal or generalized slowness. Normal EEG was recorded in 45.7% of the patients. These results are nearly in agreement with the findings of Camfield et al. [23], Shinnar et al. [27], Radhakrishnan et al. [28], Bessisso et al. [21], Winckler et al. [29], Kim et al. [5], Anang and José [19], and Rasool et al. [30], who reported that the EEG abnormality was detected in 43, 42, 50, 31, 33, 46, 43, 38.5, and 56.2% of patients, respectively. This wide variation in the results of studies may be due to differences in the time of recording EEG, as early recording within 48 h increases the rate of abnormal EEG, or due to differences in the abnormality that could be detected either epileptiform or nonepileptiform. King et al. [31] reported a higher rate of epileptiform abnormalities in EEGs performed within 24 h (51%) than those performed after 24 h (34%). An EEG performed after a seizure is more likely to detect such abnormalities, and is likely to have a greater prognostic value [32].

In the present study, the percent of recurrence among patients with abnormal EEG was 70.3% and that in those with normal EEG was 29.7%, whereas the percent of nonrecurrence among patients with abnormal EEG was 36.4% and that in those with normal EEG was 63.6%. Van Donselaar et al. [33] reported that the epileptic discharges were associated with a risk for recurrence of 83 versus 41% in patients with nonepileptic abnormalities and 12% in patients with normal EEG. Shinnar et al. [34] also reported that the risk for seizure recurrence by 24 months for children with an idiopathic/cryptogenic first seizure was 25% for those with a normal EEG, 34% for those with nonepileptiform abnormalities, and 54% for those with epileptiform abnormalities. As regards EEG abnormality, the results of the present study showed that there was a significant correlation between epileptiform abnormalities in EEG and recurrence of seizure. The recurrence of seizure occurred in 65% of patients with abnormal EEG (81% of patients with GED, 60% of patients with focal epileptiform discharge, and 42% of patients with nonepileptiform discharge) and in 26% of patients with normal EEG. These results are in agreement with those of Van Donselaar et al. [33], who reported that the finding of epileptic discharges in patients with untreated idiopathic first seizure was associated with a risk for recurrence of 83 versus 41% or 12% in patients with either nonepileptiform abnormalities or with normal EEGs, respectively. Scotoni et al. [18] reported that recurrence occurred in 27% of patients who had normal EEGs and in 60% patients with abnormal EEGs, and this was statistically significant. Wirrell [6] reported that the risk for recurrence increases from 27 to 42% if the EEG is normal and increases to 60 to 71% if epileptiform abnormalities are seen. The results of the present study showed that a significant risk for seizure recurrence was abnormal EEG, especially if the abnormality is epileptiform discharge. These results are in agreement with the findings of Rajeev et al. [35], who reported that, there are two factors that are consistently associated with an increased risk for recurrence in both children and adults: an abnormal EEG (particularly if the abnormality is epileptiform) and a symptomatic cause or abnormal neurological examination. A meta-analysis of 16 studies assessed recurrence risk after the first unprovoked seizure and showed that the strongest predictors of recurrence were seizure cause and EEG findings [36]. Pairoj [12] reported that other than epileptiform EEG and symptomatic etiology there was no significant risk for seizure recurrence. Scotoni et al. [18] reported significance for seizure recurrence only for patients with abnormal EEGs. Anang and José [19] consider abnormal EEG to be a good predictor of seizure recurrence.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

References

1Benamer H, Grosset D, Benamer H, Grosset D. A systematic review of the epidemiology of epilepsy in Arab countries. Epilepsia 2009; 50:2301–2304.
2Guidelines for epidemiologic studies on epilepsy. Commission on Epidemiology and Prognosis, International League Against Epilepsy.Epilepsia 1993; 34:592–596.
3Wilden J, Cohen-Gadol A. Evaluation of first nonfebrile seizures. Am Fam Phys 2012; 86:334–340.
4Krumholz A, Wiebe S, Gronseth G, Shinnar S, Levisohn P, Ting T et al. Practice parameter: evaluating an apparent unprovoked first seizure in adults (an evidence-based review): report of the Quality Standards Subcommittee of the American Academy of Neurology and the American Epilepsy Society. Neurology 2007; 69:1996.
5Kim L, Johnson T, Marson A, Chadwick D. Prediction of risk of seizure recurrence after a single seizure and early epilepsy: further results from the MESS trial. Lancet Neurol 2006; 5:317–322.
6Wirrell E. Prognostic significance of interictal epileptiform discharges in newly diagnosed seizure disorders. J Clin Neurophysiol 2010; 27:239–248.
7Fowle A, Binnie C. Uses and abuses of EEG in epilepsy. Epilepsia 2000; 41(Suppl 3):10–18
8Gumus H, Bayram A, Poyrazoglu H, Canpolat D, Per H, Canpolat M et al. Comparison of effects of different dexmedetomidine and chloral hydrate doses used in sedation on electroencephalography in pediatric patients. J Child Neurol 2015; 30:983–988.
9Gandelman-Marton R, Theitler J. When should a sleep-deprived EEG be performed following a presumed first seizure in adults? Acta Neurol Scand 2011; 124:202–205.
10Rubboli G, Parra J, Seri S, Takahashi T, Thomas P. EEG diagnostic procedures and special investigations in the assessment of photosensitivity. Epilepsia 2004; 45(Suppl 1):35–39.
11Hirtz D, Ashwal S, Berg A. Practice parameter: evaluating a first nonfebrile seizure in children: report of the quality standards subcommittee of the American Academy of Neurology, the Child Neurology Society, and the American Epilepsy Society. Neurology 2000; 55:616–623.
12Pairoj B. Risk of recurrence following a first unprovoked seizure in Thai children. Neurol J Southeast Asia 2003; 8:25–29.
13Martinovic Z, Nebojsa J. Seizure recurrence after a first generalized tonic-clonic seizure, in children, adolescents and young adults. Seizure 1997; 6:461–465.
14Arthur TM, deGrauw TJ, Johnson CS, Perkins SM, Kalnin Z, Austin JK, Dunn DW. Seizure recurrence risk following a first seizure in neurologically normal children. Epilepsia 2008; 49:1950–1954.
15Hirtz D, Ellenberg J, Nelson K. The risk of recurrence of nonfebrile seizures in children. Neurology 1984; 34:637–641.
16Elwes R, Chesterman P, Reynolds E. Prognosis after a first untreated tonic clonic seizure. Lancet 1985; 2:752–753.
17Hart Y, Sander J, Johnson A, Shorvon S. National General Practice Study of Epilepsy: recurrence after a fist seizure. Lancet 1990; 336:1271–1274.
18Scotoni A, Maria L, Marilisa M. Recurrence after a first unprovoked cryptogenic/idiopathic seizure in children: a prospective study from S̃ao Paulo, Brazil: Epilepsia (2004), Vol. 45,No. 2
19Anang J, José F. Single unprovoked seizure: wait time to full medical assessment, does it matter?. Neurol Bull 2012; 4:1–11.
20Davis B. Predicting nonepileptic seizures utilizing seizure frequency, EEG, and response to medication. Eur Neurol 2004; 51:153–156.
21Bessisso M, Mahmoud F, Naema A, Azzam SB, Hani A, Mariam G. Risk of seizure recurrences after first unprovoked seizure during childhood, Neurosciences 2001; 6:95–98.
22Hauser W, Rich S, Annegers J, Anderson V. Seizure recurrenceafter a 1st unprovoked seizure: an extended follow-up. Neurology 1990; 40:1163–1170.
23Camfield P, Camfield C, Dooley J, Tibbles JA, Fung T, Garner B. Epilepsy after a first unprovoked seizure in childhood. Neurology 1985; 35:1657–1660.
24Stroink H, Brouwer O, Arts W, Geerts A, Peters A, van Donselaar C. The first unprovoked, untreated seizure in childhood a hospital based study of the accuracy of the diagnosis, rate of recurrence, and long term outcome after recurrence. Dutch study of epilepsy in childhood. J Neurol Neurosurg Psychiatry 1998; 64:595–600.
25Shinnar S, Berg A. Risk of seizure recurrence following a first unprovoked seizure in childhood. Pediatrics 1990; 85:1076–2085.
26Shinnar S, O’Dell C, Berg A. Mortality following a first unprovoked seizure in children: a prospective study. Neurology 2005; 64:880–882.
27Shinnar S, Kang H, Berg A, Goldensohn E, Hauser W, Moshé S. EEG abnormalities in children with a first unprovoked seizure. Epilepsia 1994; 35:471–476.
28Radhakrishnan K, Pandian J, Santhoshkumar T, Thomas S, Deetha T, Sarma P et al. Prevalence, knowledge, attitude, and practice of epilepsy in Kerala, South India. Epilepsia 2000; 41:1027–1035.
29Winckler W, Allen H, Ettore B. First seizure definitions and worldwide incidence and mortality: Epilepsia 2008; 49(Suppl 1):8–12.
30Rasool A, Suhil A, Nisar A, Wani S, Mushtaq A, Qazi I. Role of electroencephalogram and neuroimaging in first onset afebrile and complex febrile seizures in children from Kashmir. J Pediatr Neurosci 2012; 7:9–15.
31King M, Newton M, Jackson G, Fitt G, Mitchell L, Silvapulle M, Berkovic S. Epileptology of the first-seizure presentation: a clinical, electroencephalographic, and magnetic resonance imaging study of 300 consecutive patients. Lancet 1998; 352:1007–1011.
32Rajiv M, Martin J. Early predictors of outcome in newly diagnosed epilepsy. Seizure 2013; 22:333–344.
33Van Donselaar C, Schimsheimer R, Geerts A. Value of the electroencephalogram in adult patient with untreated idiopathic first seizures. Arch Neurol 1992; 49:231–237.
34Shinnar S, Berg A, Moshe S, Petix M, Maytal J, Kang H et al. The risk of seizure recurrence following a first unprovoked afebrile seizure in childhood: an extended follow-up. Pediatrics 1996; 98:216–225.
35Rajeev S, Ram B, Rajendra A. Application of entropy measures on intrinsic mode functions for the automated identification of focal electroencephalogram signals, Entropy 2015; 17:669–691.
36Berg A, Shinnar S. The risk of seizure recurrence following a first unprovoked seizure: a quantitative review. Neurology 1991; 41:965–972.