CHAPTER

Epileptic Seizures

Matthew W. Luedke and Rodney A. Radtke

Recent advances in epilepsy and neurophysiology have naturally made the field more complex. As video electroencephalography (vEEG), continuous EEG (cEEG), and invasive EEG monitoring have developed, so too has our understanding of seizure semiology, localization, and evolution of disease (1). Revolutions in genetics, biochemistry, and functional neuroanatomy have deepened our understanding of pathophysiology, replacing descriptive distinctions among seizures and syndromes with actual etiologies and mechanism (1,2). Epileptologists have struggled to express this growing complexity with clinically and scientifically useful language.

The informal 19th- and early 20th-century categories of grand mal, petite mal, and psychomotor seizures were clinically expedient, but limited in detail. Moreover, contemporaries worried that the terms grand and petite unintentionally connoted severity, and that the tripartite categories implied a lack of overlap (3).

In the second half of the 20th century, there was a movement toward an internationally accepted nomenclature, intended to facilitate communication in clinical and research settings. The International League Against Epilepsy (ILAE) played an early role, beginning in the 1960s. In 1970, the ILAE proposed a formal classification for seizures and epilepsy, with standardized clinical and EEG criteria (4).

These original classifications were updated in 1981, but the revisions preserved the foundational language and electroclinical definitions (5). The ILAE drastically revised its terminology in 2010, opting for a more semiologic nomenclature for seizures (6). Current clinical practice tends to hybridize the two systems, and there is ongoing debate as to the practicality and validity of both systems.

This chapter will describe the two dominant schemes for seizure classification: the 1981 ILAE nomenclature for seizures and the recent 2010 ILAE guidelines. Cases will be provided to illustrate and compare the two systems in a clinical setting.

CONSIDERATIONS IN CLASSIFICATION

Classification schemes lie at the intersections of math, philosophy, and science, and can be conceptually complex; but, for the purposes of this chapter, classification will be accepted as the systematic grouping of phenomena, based off of real and meaningful differences among groups (2,7–9). Seizures represent a challenge for systematic organization. Clinically, seizures are protean, with manifestations ranging from subjective sensations to altered consciousness to convulsions. Not only are the component manifestations important, but also their sequence is critical to localization. Thus, semiology is an obvious target for classification (10).

Seizures are also described electrographically, and with the expansion of vEEG and intracranial monitoring, there are abundant electroclinical data available to characterize seizures. Electrographic characterization, like semiology, is a tempting target for seizure classification, particularly for seizures with classical electrographic morphology, like absence.

Recently, the ability to describe at least some seizure subtypes using the language of cellular and molecular biology and neural networks has helped with classification. Absence seizures, for example, are thought to be generated by abnormal T-type calcium channel function and self-sustaining derangements in thalamo-cortical circuits (11). Ostensibly, as the understanding of neuroscience expands, more subtypes of seizures will have identifiable causes at the cellular and biochemical levels, providing yet more options for categorization.

Criteria aside, the intention of a classification system is also critical. When it comes to describing seizures, clinicians have a bias toward pragmatism and generalizability. Researchers tend toward granularity and precision. The ideal would be a system that is not only user-friendly at the bedside, but also communicates detail about pathophysiology at bench (7). Such a happy medium is elusive, and has been an ongoing challenge in seizure classification.

The first attempts to classify seizures in the 1960s to 1980s brought uniformity to the language of epileptologists (4,5). This was an era of early development in seizure monitoring. Video with synchronized EEG data was newly available. Thus empowered, the committees developed an electroclinical language, based partly on the enthusiastic presumption that EEG and semiology had a direct relationship.

Somatosenory or special sensory symptoms vary depending on the region of cortical involvement and are generally positive phenomena. Primary somatosensory seizures are felt as tingling (classically described as “pins and needles”), though proprioceptive distortions can occur. As with the Jacksonian march, there can be a contiguous spread of sensation along regions subserved by the sensory homunculus. Auditory and visual seizures are variable and depend on the proportion of primary sensory and association cortex involved. They can be elementary (tinnitus or scintillations, respectively) or complex (music, formed visual hallucinations). Olfactory seizures classically tend toward unpleasant odors. Vertiginous seizures are also categorized as special sensory events, and can mimic central vertigo or generate feelings of disequilibrium.

Autonomic seizures can manifest with both general autonomic or enteric phenomenon. Tachycardia, bradycardia, flushing, piloerection, pupillary dilatation, and diaphoresis are common general autonomic manifestations. Enteric phenomenon can include emesis, borborygmi, flatus, and bowel incontinence.

Psychic epileptic symptoms have a broad range of manifestations. Dysphasia can occur with preserved consciousness, and is seen in some simple partial seizures, as are distortions of memory and recall (déjà vu, jamais vu). The guidelines subtly acknowledge “cognitive disturbances,” such as feelings of detachment, unreality, or dream states, which may preserve integrative function enough that consciousness is not impaired. Similarly, isolated affective symptoms (eg, fear), illusions (eg, macropsia), and frank hallucinations may be a manifestation of a simple partial seizure.

EEG findings defined for simple partial seizures, both ictal and interictal, are local discharges over the region of cortex subserving the clinical signs and symptoms. Of note, the guidelines acknowledge that scalp recordings often do not capture electrographic changes in simple partial seizures, making their semiology critical for their identification.

Complex Partial Seizures

Complex partial seizures can evolve either from simple partial seizures, or they can begin with altered mentation de novo. If it originates as a simple partial seizure, somatosensory, special sensory, autonomic, and psychic symptoms present prior to the onset of dyscognition are considered an aura. However, it can be difficult to judge the presence of preceding experiential symptoms because of periictal amnesia in many complex partial seizures. When originating with simple motor components, complex partial seizures can readily be described by the evolving motor phenomena.

Complex partial seizures can be further dichotomized into seizures with and without automatisms. Automatisms are complex release behaviors that emerge with the impairment of consciousness. They are learned behaviors, though they may be out of context or dyspractic, and they are also generally forgotten as part of the periictal amnesia. They can manifest as any of a number of learned motor behaviors, such as chewing, speaking, gesturing, walking, or making facial expressions. In severe complex partial seizures, they can be seen in the post-ictus as well. Automatisms can also be seen in primary generalized epilepsies, and they have limited role in localization; the guidelines do note that they are generally related to discharges in the limbic structures, but that the EEG takes precedence in localization over the presence and semiology of automatism.

Electrographically, the guidelines describe complex partial seizures as arising from unilateral or bilateral discharges frequently in the frontal or temporal regions. They can be focal or diffuse in distribution, though not overtly generalized. If there are bilateral interictal discharges, these are likely to be asynchronous.

Partial Seizure Evolving into Secondarily Generalized Seizure

Some partial seizures, whether simple or complex at onset, will evolve into a generalized seizure. The critical distinction between secondarily generalized seizures and primary generalized seizures is the focal origin with evolution to bilateral involvement. As with complex partial seizures, there is a loss of consciousness in the secondarily generalized seizure. Similarly, experiential symptoms, such as déjà vu or epigastric rising sensation preceding generalization, represent the original simple partial seizure and are considered aura. Characteristics of generalized seizures will be discussed subsequently.

Generalized Seizures

Generalized seizures are defined by clinical and electrographic onset in both cerebral hemispheres, according to the 1981 nomenclature. Consciousness alterations are often the first presentation. The guidelines note that consciousness may be impaired; though, in clinical practice, impairment of consciousness in a generalized seizure is often assumed. Motor signs are bilateral. EEG findings will be bilateral and widespread at onset, differentiating these from partial seizures with secondary generalization.

Absence Seizures

Absence seizures are characterized by a sudden behavioral arrest. Ongoing behaviors, such as speaking, eating, or walking, will either markedly slow or stop, accompanied by a blank stare. The eyes may roll upward slightly. The patient will, at least initially, be unresponsive to stimuli. The seizure will end abruptly as well. In the absence seizure with impairment of consciousness only, these are the only clinical manifestations.

The 1981 guidelines allow for the typical absence seizure to be accompanied by several subtle phenomena seen in other generalized seizure types. These phenomena can be seen individually or in combination, and their guideline descriptions are summarized in the following. The absence seizure with mild clonic components has all the characteristics of altered conscious noted earlier; however, there are clonic motions that can be seen, usually in the eyelids and mouth. When they involve the limbs, the patient can drop or throw objects held at the onset of the seizure. These clonic movements can manifest on a spectrum from the almost imperceptible to outright myoclonic jerks. Absence seizures with mild atonic components demonstrate minor losses in tone, leading to weakness usually in nuchal or trunk muscles, but sometimes also in the limbs. Unlike atonic seizures, where loss of tone can be sudden, these manifest as a drifting of limbs, neck, or trunk, and rarely as falls. Absence seizures with tonic components generate increased extensor or flexor tone in the neck, trunk, or limbs, and can cause back arching or retropulsion. Absence seizures with automatisms demonstrate automatisms comparable to those discussed with complex partial seizures. Indeed, in younger patients with new-onset epilepsy, absence seizures with automatism can be challenging to differentiate from complex partial seizures with automatisms on clinical grounds, often benefitting from EEG to differentiate. Absence seizures with autonomic components occur in conjunction with autonomic symptoms consistent with those discussed in simple partial seizures.

EEG criteria for absence seizures are a unifying feature. They consist of regular, rhythmic 2 to 4 Hz (classically, 3 Hz) spike–slow-wave discharges, which are bilateral and generally symmetric. The interictal EEG is generally normal, with the exception of generalized burst phenomena, which can range from slowing to spike-wave activity.

Atypical Absence Seizures

Atypical absence seizures are similar to typical absence seizures, but have both semiologic and electrographic aberrations. Clinically, they can have prolonged, or evolving onsets and endings, rather than beginning or ending abruptly as in typical absence. When tonic components are present, these, too, are more pronounced.

Electrographically, atypical absence seizures are defined by irregularity in the normally very rhythmic spike–slow-wave complexes, along with other high-frequency bursts and paroxysmal discharges. Seizures and paroxysms are often asymmetric, though still bilateral. There is more paroxysmal activity in the interictal EEG, often with asymmetric spikes and spike–slow-waves, and background activity is typically abnormal in these patients. The abnormal background is expected, given that atypical absence seizures usually are seen in patients who have multiple seizure types (eg, tonic and atonic) and have significant cognitive impairment.

Myoclonic Seizures

Myoclonic seizures are sudden, short-duration contractions of muscles in the face, limbs, or trunk. They can be isolated, or occur in trains or clusters of jerks. Myoclonic jerks can be epileptic, relating to abnormal cortical activity, frequently in association with epilepsy syndromes, classically JME. However, myoclonus is frequently nonepileptic, arising from other sites in the central nervous system. Caution must be taken in diagnosing epileptiform myoclonus.

EEG findings associated with myoclonic seizures are typically polyspike-and-wave, spike-and-wave, or spike–slow-wave activity. Interictal EEGs can be normal, though tend to demonstrate interictal bursts of spike-wave or polyspike-wave activity.

Tonic Seizures

Tonic seizures present with sudden and fixed contractions of limb, trunk, neck, and facial muscles. Contractions can be asymmetric, with eye and head deviation, and even turning of the body, along with uneven posturing of the limbs. As the muscles of the trunk contract, patients can become apneic, with pallor or cyanosis. Tonic activity can either be the principal semiology of a seizure, or occur as a phase in a longer ictus.

Electrographically, tonic activity generally appears as generalized alpha, or low-voltage fast activity, which increases in amplitude and decreases in frequency as the seizure evolves. Interictal EEGs are generally abnormal at baseline; spike-slow-wave discharges can be seen as well.

Clonic Seizures

Clonic seizures appear as alpha or beta frequency discharges, sometimes with spike-wave morphology. As the clonic motor activity slows, the EEG waveforms slow. The interictal EEG will frequently manifest spike-wave or polyspike bursts.

Tonic–Clonic Seizures

As noted, tonic and clonic seizure activities are often phases of a more complex seizure. In the tonic–clonic seizure, classically called a grand mal, the seizure will begin with a tonic phase, which evolves into clonic activity. The tonic and clonic phases are consistent with the activity described in pure tonic or clonic seizures, and can frequently be accompanied by tongue biting and incontinence. The postictus can be profound, accompanied by somnolence, flaccidity, and prolonged confusion.

The tonic-phase EEG is accompanied by high alpha or beta frequency activity building in amplitude. With the clonic phase, the high-frequency activity is interrupted by a rhythmic spike-wave activity, which slows along with the clonic movements. A variant is the clonic–tonic–clonic seizure, which, as implied, starts with a clonic phase, progresses through a tonic phase, and concludes by returning to clonic activity. The interictal EEG is frequently abnormal, with polyspike-and-wave, spike, or spike-slow-wave activity.

Atonic (Astatic) Seizures

Essentially a semiologic inverse of the tonic or clonic seizures, the atonic or astatic seizure is a sudden reduction or loss of muscle tone. They can be focal or generalized, involving the face, neck, trunk, or limbs. The onset can be gradual, leading to a progressive slumping or slouching. This slow-onset process can occur in a stepwise manner, as successive, rhythmic relaxations of the muscle groups. Fast-onset atonic seizures, the classic “drop-attack,” can lead to falls and head or neck injuries.

Atonic seizures are electrographically variable. They can appear as burst of polyspike activity or as electrodecrement, a flattening of the background, often after a generalized discharge. The interictal EEG is often abnormal, and can contain polyspikes, slow waves, and other generalized discharges.

Unclassified Epileptic Seizures

At the time the 1981 recommendations were published, the authors recognized that many seizure types, often those seen in neonates, did not fit their classification scheme. These seizures were left undefined, with the understanding that further EEG and semiological data could eventually lead to their formal classification.

THE 2010 RECOMMENDATIONS FOR CLASSIFICATION OF SEIZURES

The 1970 and 1981 proposals for seizure classification were a marked improvement over the more traditional terminology of petite mal, grand mal, and psychomotor epilepsy. Testing of the nomenclature in practice has shown promise, but some challenges as well. For example, it has been shown that even trained lay evaluators could accurately identify many seizure types, most reliably partial seizures, along with complex partial seizures and generalized tonic–clonic seizures. Interrater reliability was good between lay scorers and neurologists, though results were poor when scoring for simple partial, myoclonic, and atonic seizures (13). However, in the authors’ experience, there remains confusion regarding absence and complex-partial epilepsy among nonneurologists, and lay observes frequently default to more traditional grand and petit mal terminology.

Implementation and adoption aside, there are several technical problems with the electroclinical classification scheme. First, semiology and electrographic manifestations do not always directly correlate; this is especially true in frontal lobe seizures, which eluded precise clinical descriptions into the 1980s.

Furthermore, since electrographic and anatomical abnormalities did not always correlate, several prominent epileptologists argued that a purely semiologic nomenclature would be more appropriate (10,14,15).

Second, with improving structural and functional imaging, the classical distinction of a focal and generalized seizure became murky. The generalized seizure came to be seen as a focal process, rapidly conducted along a widespread, bilateral network of neurons; the partial seizure, conversely, originated from a focal region and spread more slowly, though not necessarily less widely, along different networks (15). With the idea of networked seizure propagation, the traditional dichotomy of a partial and generalized seizure was less reliable.

Third, the classification of partial seizures based off of alterations in consciousness was called into question. While, medico-legally, an alteration in consciousness has bearing on the ability to drive; it does not necessarily correlate with seizure severity or localization. Also, alterations in consciousness can be difficult to identify, particularly with ictal manifestations effecting individual components of consciousness. Returning to the operating definition, classification should be based off of meaningful differences between groups; to many epileptologists, it is unclear if altered mentation is a meaningful distinction (16).