Sensitivity and specificity of surface scalp EEG to localize the epileptogenic focus depends on factors such as age, type of epilepsy, and nature of EEG recording [2]. Ictal EEG (EEG recording during the seizure) helps to recognize the type of seizure that may not be evident from history and for localizing the epileptogenic zone [3]. Electrocorticography (ECoG) or intracranial EEG is useful for invasive recording of cortical electrical activity by use of electrodes directly on the surface of brain (subdural grids or strips) or deep inside the brain (depth electrodes) [4]. It helps to localize the epileptogenic zone and to map cortical functional areas in drug-resistant epilepsy. Detailed discussion of invasive EEG studies and its role in planning epilepsy surgery is beyond the scope of this review. American Clinical Neurophysiology Society (ACNS) has published technical guidelines for recording digital EEG [5].

EEG measures the electropotential difference that arises from the ion trafficking between two points on the scalp. Potential differences between electrodes are amplified and the net signal from each amplifier is displayed on a monitor to provide a graphic record. EEG signals are generated by the summation of excitatory and inhibitory post-synaptic potentials from large, vertically-oriented pyramidal neurons located in layer III, V and VI [6]. These EEG signals are synchronized by subcortical structures like thalamus and brainstem reticular formation. Sleep spindles are considered a result of these thalamocortical phenomena [6]. Large numbers of cortical spikes are not recordable on a routine scalp EEG due to attenuating effect of cerebrospinal fluid, duramater and skull scalp tissue.

The surface EEG electrodes made of gold or silver discs (silver chloride) are placed at standard points over scalp with a conductive paste. The International 10-20 system (10 and 20% gap between electrodes) is used for electrode placement [7]. Pediatric EEG routinely requires the placement of 21 electrodes on the scalp with fewer electrodes (minimum of 12 electrodes) in neonates and young infants [8]. EEG can be performed in a laboratory or bedside ambulatory EEG could be used. Additional channels of electrocardiogram (EKG) and respiration are recommended to record physiologic artefacts. EKG during EEG recording helps detect ictal arrhythmia and asystole in children with epilepsy who are prone to sudden unexpected death (SUDEP) [9]. Surface electromyography (EMG) during EEG helps to distinguish epileptic from non-epileptic movements [10]. Electrodes are named according to the underlying area of brain: FP: frontopolar, F: frontal, P: parietal, T: temporal, and O: occipital. Central electrodes are abbreviated as Z [Fz, Cz, Pz] and referential electrodes include post auricular (A1, A2). The odd numbers (Fp1, F3, P3, C3, T3, T5, T7, O1) depict left side of the hemisphere and even numbers (Fp2, F4, C4, P4, T4, T6, O2) for the right side. These electrodes are either fixed to scalp using conductive paste or electrodes fixed onto a head cap are used.

The scalp should be clean and dry. Patient should be instructed to consume antiepileptic drugs (AED) as prescribed. However, AED doses can be reduced or discontinued to facilitate seizure occurrence during long-term video EEG monitoring [11]. Children can have their routine breakfast on the day of appointment. Routine EEG recordings usually lasts for 30 minutes, including hyperventilation for 3 minute and intermittent photic stimulation at 1-30 Hz [5]. Long-term video EEG recordings are particularly useful for pre-surgical evaluation for epilepsy surgery [12]. An ideal EEG should include both awake and sleep record. However, sleep EEG is preferred in younger children considering excessive movement artefacts during the wakeful state. Moreover, sleep EEG provides vital information on maturation of brain [8]. Sleep deprived EEG protocol requires 4-6 hours of sleep deprivation [13]. Children older than 3 years could be kept awake until midnight and woken up at 5:00 AM on the morning of the test. Sleep deprivation is considered to enhance sensitivity of EEG [14]. Triclofos (20 mg/kg/dose), melatonin (2-6 mg/dose) or clonidine (0.05-0.2 mg) can be used for sedation [15]. Intravenous midazolam should not be used to induce sleep due to its suppressive effect on epileptiform discharges. In addition to sleep deprivation, yield of EEG can be increased by repeat recording, prolonging the duration of recording, increasing the number of channels during procedure, simultaneous video recording, and recording both awake and sleep state [16].

Infants, young children and children with suspected focal epilepsies require sleep EEG record [17-19]. Sleep EEG is essential for diagnosis of epileptic encephalopathy and continuous spike waves during slow sleep (CSWS) [20]. EEG in awake state is useful to detect generalized epilepsies. Activation procedure include hyperventilation (3 Hz spike wave pattern in absence epilepsies) and intermittent photic stimulation (4-6 Hz generalized epileptiform discharges in Juvenile myoclonic epilepsy). Other activation procedures indicated for specific conditions are: fixation of sensitivity (late onset occipital lobe epilepsy), precipitation by trigger (e.g., video watching) in reflex epilepsies, and suggestion to precipitate paroxysmal non-epileptic events [21]. Reactivity of EEG background is observed by asking the child to close and open the eyes or by touching his various body parts.

An EEG requisition form from clinician must contain basic demographic profile (name, age, gender, telephone number or email), type of seizure, frequency of seizure, age at onset, indication of EEG, neuroimaging findings, any previous EEG findings, and name of antiepileptic drugs. Neurophysician can decide on the EEG protocol based on clinical diagnosis. For example, in a child with suspected absence epilepsy, one would prefer an awake EEG record with hyperventilation. Sleep deprived sleep EEG record will be considered in a child with suspected focal epilepsy.

ACNS guidelines have outlined five essential components of an EEG report (Table I) [22]. Abnormalities in EEG can be divided into background abnormalities and abnormal epileptiform discharges. Background gives information about the neurologic state of the child. Normal awake record consists of posterior dominant alpha rhythm (8-13 Hz) with reactivity to eye closure. Similarly, sleep background consist of sleep markers of non-REM sleep such as sleep spindles, vertex waves, and K-complexes (Web Fig. 1). Epileptiform discharges have distinct waveforms classified as spikes (<70 ms) or sharp wave (70-200 ms). EEG findings in common self-limited epilepsies and epileptic encephalopathy in children have been summarized in Table II and Table III, respectively.

TABLE I Essential Component of an Eeg Report (as per Acns Guidelines for Reporting Eeg).

TABLE II Clinical and EEG Findings in Self-limited Epileptic Seizures and Syndromes

 

TABLE III Clinical and Eeg Features of Epileptic Encephalopathy

Pitfalls of EEG

Surface EEG can be normal in few epileptic conditions in children, especially those with remote and deep location of epileptogenic lesion such as interhemispheric area, and mesial and basal cortex [19]. Few genetic types of epilepsy such as benign familial neonatal epilepsy and benign familial infantile epilepsy can have normal interictal EEG. Epileptiform discharges are found in 0-5.6% of normal healthy children and 0.5% of adults without any event of seizure [23]. EEG can be abnormal in approximately 5.7-59% of children with autism spectrum disorder without any clinical seizures [24]. Photic driving response can routinely be found in patients with migraine without any epilepsy [25]. EEG is often reported by neurologist, pediatric neurologist, psychiatrist, neurophysiologist and other physicians with interest in EEG. Hence, there is lot of variability and subjectivity in reporting pediatric EEG. Exclusive training and experience to interpret pediatric EEGs is essential to understand the normal age-dependent variations and correct characterization of epileptiform discharges. Some of the common errors in pediatric EEG reporting include misinterpreting movement artefacts, high amplitude delta slowing during hyperventilation and normal sleep markers including vertex waves, and K complexes as epileptiform discharges (Web Fig. 1). Other benign epileptiform variants like wicket waves, benign epileptiform transients of sleep (BETS) and rhythmic midtemporal theta bursts of drowsiness (RMTD) can mimic epileptiform discharges to a naïve reader [26]. Awake EEG record can be normal in children with suspected rolandic epilepsy, structural focal epilepsy or CSWS. These abnormalities are detected only on sleep EEG record. Similarly, among those with suspected childhood absence epilepsy and juvenile myoclonic epilepsy, hyperventilation and photic stimulation during awake EEG record is mandatory.

EEG is an adjunct to clinical evaluation and should be interpreted in clinical context. Indications of using and not using EEG are summarized in (Box 1). Diagnosis of epilepsy should not be reached solely on the basis of EEG findings [27]. A wrong diagnosis of epilepsy has widespread social implications apart from side effects of antiepileptic drugs and restriction of physical activities. EEG is often misused in evaluation of a child with abnormal paroxysm to differentiate epileptic from non-epileptic event [28]. Over-interpretation of EEG abnormalities, including focal slowing, generalized and focal epileptiform discharges has often led to syncope being misdiagnosed as epileptic seizures [21]. There is limited role of EEG in children with breath holding spells. Common reasons for misinterpretation of EEG include poor expertise, lack of good quality recording, inappropriate indication, and absence of clinical correlation [27]. Routine surface scalp EEG report should ideally comprise five components: history, technical description, EEG description, impression and clinical correlation [22].

First unprovoked seizure (FUS) is defined as first non-febrile seizure that cannot be explained by an immediate, obvious precipitating cause such as head trauma or intracranial infection. In developing countries including India, focal lesions such as neurocysticercosis (NCC) and tuberculoma are common causes of first unprovoked seizure in children [29]. Thus, in many centers, neuroimaging often precedes EEG in evaluation of such children. EEG is recommended as first tier investigation among children with first unprovoked seizure for diagnosis of seizure, epilepsy type and an epileptic syndrome. It may be useful for prediction of long-term outcome or recurrence [30]. Children who have focal epileptiform discharges on EEG have a higher risk for recurrence when compared to those with normal EEG [31]. However, in obvious etiology like neuro-cysticercosis or tuberculoma, EEG should not be routinely requested at outset. EEG may be helpful before withdrawing AED in such patients. Among children with new onset seizures, 18-56% display epileptiform discharges on initial EEG and 15% will never show abnormal findings [32]. EEG done early within first 24 hours of seizure shows background and epileptiform abnormality more frequently [33]. These background abnormalities are often transient and warrant repeat EEG after certain duration to look for persistence of abnormality.

EEG abnormalities are broadly divided into background abnormalities and abnormal epileptiform waveforms. Background abnormalities include diffuse slowing, asymmetric slowing, discontinuous background and electrodecremental response. Group of disorders with discontinuous EEG background where epileptiform activities contribute to encephalopathy or non-attainment of milestones is called epileptic encephalopathy. This includes Early myoclonic encephalopathy, Ohtahara syndrome, West syndrome (Web Fig. 2), Lennox Gestaut syndrome, and Landau Kleffner syndrome. There are signature EEG features to diagnose epileptic encephalopathies as these conditions have urgent treatment implications (Table III). Interictal EEG can be categorized into focal or generalized based on the morphology of epileptiform discharges and organization of background activity. Generalized spike and spike-wave discharges with normal interictal background activity is observed in childhood/juvenile absence epilepsy (CAE/JAE), epilepsy with myoclonic astatic seizures (Doose syndrome), juvenile myoclonic epilepsy (JME) (Web Fig. 3), and epilepsy with eyelid myoclonia (Jeavon syndrome). There are a group of self-limited epilepsies with focal stereotyped spikes wherein the focal spikes can be seen with normal interictal EEG background. This includes Rolandic epilepsy (Web Fig. 4), Panayiotopoulos syndrome and benign occipital epilepsies. Children with structural lesion like Neurocysticercosis, glioma or vascular lesion can also have focal epileptiform discharges (Web Fig. 5). Children with subacute sclerosing panencephalitis can have periodic epileptiform discharges (Web Fig. 6).

EEG is required to rule out nonconvulsive status epilepticus among those with no improvement of altered sensorium following convulsive seizures [34]. EEG is also useful adjunct to monitor seizure activity among those with neuromuscular blockade (which might mask convulsive activity) and high dose suppressive therapy for refractory status epilepticus. Among those with refractory status epilepticus, suppression of epileptiform discharges to achieve burst suppression on EEG is often considered end point for titrating the dose of antiepileptic and anesthetic agents [35].

Continuous EEG monitoring in intensive care unit (ICU) setting is ideal during management of a child with refractory status epilepticus, heavy sedation, those on neuromuscular blocker, or those being treated with barbiturate for raised intracranial pressure [36]. A comatose child with past history of seizure or seizure like activity requires an EEG to rule out non convulsive status epilepticus. The most common EEG finding in a child with coma is diffuse slowing with reduction in amplitude of waveform. Triphasic waves on EEG could point to ward underlying metabolic disorder. Similarly, periodic lateralized epileptiform discharges (PLED) suggest a focus of irritable cortex seen in space occupying lesion or herpes encephalitis. Serial EEG can help with prognostication. In children with post anoxic coma, burst suppression or isoelectric pattern on EEG is a poor prognostic marker for recovery [37]. EEG monitoring in ICU setting has limited role because of environmental noise and use of sedative drugs.

There is no role of EEG in children with simple febrile seizures [38]. However, EEG is more likely to be abnormal among those with complex febrile seizures, including febrile status epilepticus and focal febrile seizures. Focal epileptiform abnormalities were significantly more frequent among children with complex febrile seizure who subsequently developed epilepsy [39]. However, epileptiform EEG has poor positive predictive value for subsequent development of epilepsy [40], and there is no evidence to support or refute the use of EEG after complex febrile seizure [41]. Hence, there is limited utility of EEG among children with febrile seizures with lack of clinical significance of an abnormal EEG in predicting recurrence or subsequent development of epilepsy.

Majority of children who are seizure-free for a duration of at least 2 years or more have minimal risk for seizure recurrence [42]. However, the risk of recurrence following withdrawal will depend on type of epilepsy, polytherapy, abnormality on neuroimaging and EEG [43]. Patients with intellectual disability, abnormal neurological examination, older age at onset of seizure, focal seizures and epileptiform abnormalities on EEG have a higher risk of relapse [42]. Abnormal EEG at the time of AED withdrawal has been shown to be associated with a relative risk of recurrence of 1.45 (95% CI 1.18-1.79) [44]. There is an emerging interest on serial EEG monitoring during AED withdrawal to predict risk of recurrence. In a study on 84 children who had seizure recurrence despite normal EEG at the time of drug withdrawal, 24 had abnormal EEG during AED withdrawal [45].

A normal interictal EEG does not exclude the diagnosis of epilepsy. EEG is useful to establish the diagnosis of epilepsy, classify the type of epilepsy and to rule out nonconvulsive status epilepticus among children with unexplained coma. EEG is often misused to justify the need for AED among children with clear history of paroxysmal non-epileptic events, headache, simple febrile seizures and head trauma. An abnormal EEG report should always be interpreted in clinical context.

Acknowledgments: Dr Suvasini Sharma and Dr Rachana Dubey Gupta for their suggestions in improving the manuscript; and Prof Kiran Bala and Prof Surekha Dabla, Department of Neurology, PGIMS, Rohtak for their guidance in the manuscript and for providing images of EEG tracings.

Contributors: Both authors contributed to review and synthesis of literature, manuscript writing, and final approval of the version to be published.

Funding: None; Competing Interest: None stated.

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