Early observers of epileptic seizures noted that seizure symptomatology could shed some insight into the underlying epileptic process, with focal seizures (e.g., right arm clonic jerking) tending to occur in patients with focal lesions (e.g., remote traumatic injury to the left perirolandic region) and bilateral or generalized seizures (generalized myoclonic jerks) being associated with more generalized processes. These observations suggested a strong correlation between the clinical features of seizures and the underlying epileptic process or syndrome. With the advent of electroencephalography (EEG) in the 1930s, however, it became clear that similar or identical clinical seizure types could be present in patients with either generalized or focal EEG abnormalities. For example, episodes of staring and loss of consciousness could occur with either generalized 3-Hz spike-wave complexes or anterior temporal sharp waves.

Continued research identified various electroclinical syndromes considered essential for diagnosis of the epilepsy syndrome. This philosophy dominated during the development of the 1964 ICES, which used terms derived from descriptions of symptomatology to characterize electroclinical syndromes. The 1981 ICES added new terminology that divided seizures into focal or generalized types on the basis of electroclinical features. For example, seizures characterized by staring and impaired consciousness were called “absence” if the patient’s EEG features were generalized and “complex partial” if the EEG features were focal. This approach reflected the assumption that a strict one-to-one relationship exists between the electroclinical syndromes and the corresponding epilepsy syndromes.

Although EEG features are an integral part of the 1981 ICES, they are not always available in clinical practice. Routine interictal EEG may not be revealing, and only a small minority of patients with epilepsy undergo prolonged video-EEG recording. In these cases, assumptions are often based on other lines of evidence. In a patient with no interictal epileptiform discharges on EEG, for example, episodes of loss of consciousness are assumed to be complex partial seizures if magnetic resonance imaging (MRI) shows a temporal lobe tumor. If neither test is revealing, or before any test has been performed (as may be the case at a patient’s initial visit), the focal or generalized nature of the epilepsy may not be
apparent solely from a description of the seizures. In this situation, precise use of the 1981 ICES is not possible.

Moreover, the electroclinical approach does not allow for easy expression of many potentially important seizure signs and symptoms. By focusing heavily on the presence or absence of altered consciousness as the key distinction between complex or simple types of focal seizures, the 1981 ICES deemphasizes much of the rich symptomatology that may carry localizing or lateralizing significance. The ictal level of consciousness may be difficult to determine and offers little localizing information, because seizures with or without loss of consciousness may arise from any region of the brain. Other seizure signs or symptoms may greatly enhance epileptogenic localization, but they are not easily expressed in the 1981 ICES. For example, the 1981 classification offers “simple partial seizure with focal motor signs,” whereas a clearer and more informative description might be “left arm clonic seizure.” A classification system encompassing a broad range of seizure symptomatology would be especially valuable to neurologists evaluating patients for epilepsy surgery, because convergence of data from different lines of testing is key to localization of the epileptogenic zone.

Recently, it has become clear that a strict one-to-one relationship between electroclinical syndromes and the corresponding epilepsy syndromes does not exist. Modern neuroimaging has allowed neurologists to identify important etiologies in vivo, such as cortical dysplasia and hippocampal sclerosis, that were previously often found only on histopathologic analysis. Correlation of neuroimaging and video-EEG results demonstrates the variable relationship between an electroclinical syndrome and the underlying epileptogenic process (15), especially among infants (16) in whom interrater agreement for seizure classification according to the 1981 ICES proved to be poor (17). Whereas focal epilepsy in children and adolescent seems to present with features commonly associated with focal seizure onset—for example, auras and clonic jerking of one extremity—infants frequently exhibit either subtle motor signs only or symmetric tonic movements commonly thought to be associated with generalized epileptogenicity (18,19). Infantile spasms and hypsarrhythmia, traditionally thought to correspond to a generalized epilepsy syndrome, may be due to a focal brain lesion identified on MRI (20, 21, 22). At this point, assumption of a one-to-one relationship, as in the 1981 ICES, leads to confusion between the classification of epileptic seizures and epilepsy syndromes.

In an effort to avoid these limitations, Lüders and colleagues (16,23, 24, 25, 26, 27) have proposed a seizure classification system based solely on the main signs and symptoms of the seizures identified by a patient or by a direct observer, or by analysis of ictal videotapes. This system, which has been used at selected epilepsy centers for more than 10 years, has several advantages.

“Unbundling” the signs and symptoms of seizures from EEG, neuroimaging, and other clinical information allows them to contribute independently to the diagnosis of an epilepsy syndrome. The assignment to generalized or focal pathophysiology is thus deferred until the entire clinical picture—available results from family history, a patient’s past and present history, neurologic and physical examination, seizure symptomatology, EEG, neuroimaging, and genetic testing—can be considered together. This system emphasizes the importance of a diagnosis of epilepsy syndrome in every case, because symptomatology alone provides limited information about the best choice of antiepileptic drugs, prognosis, need for neuroimaging, and other therapeutic considerations. This type of seizure classification is similar to classification systems used in other fields of neurology. For example, in a patient with tremor, the movement disorder syndrome is the essential diagnostic end point, not the tremor itself.

Keeping seizure symptomatology separate from other clinical and laboratory features eliminates the current confusion between electroclinical complexes and epilepsy syndromes, thus emphasizing the importance of symptoms and focusing attention on their role in a diagnosis of epileptic syndrome. Such a system, which encourages research into the types of ictal signs and symptoms observed in different epilepsy syndromes and vice versa, can be applied in the absence of MRI or EEG abnormalities.

The seizure classification system proposed by Lüders and colleagues places ictal signs and symptoms into one of four domains: sensation, consciousness, autonomic function, or motor function (Table 14.1).

Seizures characterized by sensory or psychic disturbances without loss of consciousness or other features are called auras; seizures characterized by abnormal movements, with or without loss of consciousness, are known as motor seizures; seizures with predominantly autonomic (i.e., involuntary) features are considered autonomic seizures; and seizures in which prominent feature is loss of consciousness are referred to as absence, or dileptic, seizures. Knowledge of the focal or generalized nature of the epilepsy is not required for this classification. For example, absence (or dileptic) seizures characterized by quiet unconsciousness may be seen in childhood absence epilepsy, as well as in some cases of frontal or temporal lobe epilepsy. The neutral but unfamiliar term “dileptic” was proposed to avoid confusion with the traditional use of “absence” as an electroclinical syndrome.

Motor seizures are subdivided into simple and complex types. In simple motor seizures, unnatural and apparently involuntary motor movements are similar to those elicited by electrical stimulation of the primary motor areas. Simple motor seizures may be further subdivided into clonic, tonic, tonic-clonic, myoclonic, and versive seizures, and epileptic spasms. In complex motor seizures, the relatively complicated movements simulate natural movements but are inappropriate for the situation. The term “complex” here does not mean that the patient necessarily loses awareness during the seizures, although impaired consciousness is common. Complex motor seizures may be further subdivided into automotor seizures with repetitive oral or gestural automatisms, often seen in temporal lobe epilepsy; hypermotor seizures with dramatically increased behavioral movements, which sometimes occur in seizures arising from mesial or orbitofrontal regions; and gelastic seizures with inappropriate or mirthless laughter, typically seen with hypothalamic hamartoma.

Seizures that do not fit into other categories, including those characterized by “negative” or “inhibitory” features, are classified as special. Atonic seizures involve loss of postural tone, resulting in head drops or limp falling. Astatic seizures consist of epileptic falls. Videopolygraphic studies show that these may be caused by pure atonia, atonia following a myoclonic jerk, or pure tonic stiffening, but in clinical practice, the exact pathogenesis is often unclear. Hypomotor seizures are characterized by decreased or absent behavioral motor activity without the emergence of new motor manifestations; this descriptive term is useful for infants or severely mentally impaired individuals, in whom it is not possible to test consciousness directly (16,28). Akinetic seizures are characterized by the inability to perform voluntary movements despite preserved consciousness, as may occur with activation of the negative motor areas in the mesial frontal and inferior frontal gyri. Negative myoclonic seizures consist of a brief interruption of tonic muscle activity caused by an epileptiform discharge; the resulting brief, sudden movement is caused by loss of muscle tone. During aphasic seizures, the patient cannot speak and often cannot understand spoken language. Aphasic seizures may be a negative phenomenon induced by the epileptic activation of a cortical language center, similar to that induced by electrical stimulation of cortical language areas.

Modifiers may be added to express the somatotopic distribution of ictal signs and symptoms, as, for example, “left-hand clonic seizure” or “generalized clonic seizure.” Modifiers refer to the part(s) of the body involved in the seizure, not to the side or lobe of the brain generating the ictal discharge. To express the evolution of symptoms that occurs as the seizure discharge spreads to new cortical areas, the components can be listed in order of appearance and linked by arrows (see examples below).

Examples:

Verification of the state of consciousness is necessary only for some specific seizure types, such as dileptic seizures, in which loss of consciousness is the predominant symptom, and auras, in which consciousness is always preserved. However, the state of consciousness may be an important semiological variable. The semiological seizure classification allows for the specification at which point in the sequence of symptoms the patient lost consciousness by inserting the expression “loss of consciousness” (LOC) after the seizure component during which consciousness was lost.

There are several semiological features of the ictal or postictal state that are not necessarily the main element of a seizure component, but have been established as reliably lateralizing the hemisphere of seizure onset—for example, dystonic posturing (29), ictal speech (30), or postictal weakness (31). These lateralizing signs can be listed following the seizure sequence.

This system permits classification of seizures with different degrees of precision to match the available information. If information is limited, as in the absence of a witness or a complete or accurate history, a less detailed classification may be appropriate (e.g., “motor seizure”). Progressively greater amounts of information may permit further categorization of the seizure as “simple motor,” “right arm motor,” or “right arm clonic.”

The 1981 ICES, which defines epileptic syndromes on the basis of electroclinical syndromes, has provided a common language for the advancement of patient care and research. However, the authors of the 1981 ICES revision expected (and actually hoped for) further revisions of the classification, as they were aware that increasing knowledge would lead to modification of their approaches and concepts (13). Recent advances in neuroimaging and molecular biology have revolutionized the definition of epileptic syndromes, providing insights beyond those obtained from EEG alone and demonstrating that a strict one-to-one relationship between electroclinical syndromes and the underlying epileptic processes does not exist. In addition, an alternative seizure classification system based solely on symptomatology has been proposed by Lüders and colleagues (23, 24, 25, 26). As a result of those developments, the Commission on Classification and Terminology of the ILAE is revising the classification (14).