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The Electroencephalogram in the Evaluation of Seizures: Current Clinical Applications
The Electroencephalogram in the Evaluation of Seizures Current Clinical Applications DONALD W. KLASS, M.D.
Where there is much desire to learn, there of necessity will be much arguing, much writing, many opinions . ... JOHN MILTON: AREOPAGITICA
Much has been written, much has been argued, and many opinions have been expressed about the role of the electroencephalogram (EEG) in the evaluation of seizures. Indeed, we have learned a great deal since the advent of electroencephalography, as Milton might have wished. With accumulation of new information, however, opinions change; and periodic reassessment of current practice can sometimes be helpful for continued learning. In the past, considerable misunderstanding has arisen with regard to the usefulness of the EEG in diagnosis of convulsive disorders. Some clinicians have expected the test always to furnish a complete diagnosis and an outline for treatment, while others have considered it of no value whatever in the evaluation of seizures. Both viewpoints are erroneous. For comprehensive evaluation of any seizure, it is desirable to know its site of origin in the brain, the pathologic process that produces it, and the nature and mode of propagation of the electrical discharge, as well as the details of the clinical manifestations. Used properly, the EEG should be important in developing part of this knowledge. It can be regarded as an extension of the traditional neurologic examination.
EEG PATTERNS-THEIR TERMINOLOGY AND CLINICAL IMPLICATIONS When electroencephalography was first being developed, there were those who hoped that the electrical activity recorded through the intact skull and scalp would show a distinctive alteration for each type of clinical seizure, and some constant alteration to indicate the presence of a convulsive disorder between attacks. Unfortunately, these hopes have not been substantiated, for there is not a particular type of electrical abMedical Clinics of North America- Vo!. 52, No. 4, July, 1968
949
950
DONALD
W.
KLASS
NORMAL
NON SPECIFIC DYSRHYTHMIA
SPIKE AND WAVE
MULTIPLE SPIKE AND WAVE
~,~~~z SPIKE I
DELTA
!too ."."
Figure 1. Typical EEG patterns.
normality corresponding to each type of clinical attack, and between attacks the usual means of recording cannot always reveal an abnormality. The technical aspects of the EEG will not be considered here in detail, but their importance should not be underestimated. Proper recording and interpretation of the EEG require special training and extensive experience. The misinformation resulting from ignorance of the many possible technical pitfalls can be of more serious consequence than the lack of information in the absence of any test at all." Some types of interictal EEG patterns are often termed "specific" or "epileptiform," since they have a distinctive morphology and appear in a high proportion of records from patients with seizures but rarely in records from asymptomatic persons. Examples of such patterns include certain types of spikes, sharp waves, and spike-and-slow-wave complexes (Fig. 1). These patterns in the EEG allow prediction of a clinical convulsive disorder with a high degree of probability. Not all types of spikes or spike-and-wave patterns, however, have similar implications. The 14- and 6-per-second positive spikes, small sharp spikes and 6-persecond spike-and-wave complexes, for example, have a different significance (and the first two of these are considered in more detail elsewhere in this issue-see p. 941). Bursts of sinusoidal waves of abnormally slow frequency (less than 8 cycles per second) or non"'To help assess the qualifications of an electroencephalographer, the reader may wish to consult the lists of electroencephalographers certified by the Board of Qualifications of the American EEG Society, which are published in the Journal of Electroencephalography and Clinical Neurophysiology. Lists of technicians being certified by the recently formed American Board of Registration for Electroencephalographic Technologists are published in the American Journal of EEG Technology.
THE ELECTROENCEPHALOGRAM IN THE EVALUATION OF SEIZURES
951
paroxysmal aberrations of frequency are usually termed "nonspecific" (Fig. 1).5 Although these changes may appear in records from patients with seizures, they are also recorded frequently from patients with other symptoms or occasionally from asymptomatic persons; and they lack a distinctive morphology. Despite the high probability of association between some EEG patterns and clinical manifestations, the correlation is not perfect. Designation of EEG patterns by clinical terms such as "grand mal discharge" or "petit mal discharge" should be avoided, since the individual patient may have had another type of attack or-an even more disturbing discrepancy-no clinical seizures at all. Furthermore, the significance of many EEG patterns depends upon the age of the patient at the time of recording. Some types of focal spike activity, for instance, may appear transiently during childhood without overt manifestations, whereas similar activity in a record from an adult would generally have a higher correlation with clinical seizures and stable focal lesions. The relationship between particular symptoms and interictal EEG abnormalities is therefore not absolute, but rather an association of varied probability, dependent upon the nature of the symptoms and the character of the different EEG patterns. The most convincing proof of the epileptic nature of particular clinical symptoms or behavior is obtained if they occur during the EEG recording at the same time as a definite ictal EEG abnormality. This may be the only way to establish the nature of the disorder if the patient cannot or will not relate his symptoms adequately and if an attack has not been observed, or if the attack seems atypical. The absence of epileptiform discharge in a single EEG record does not exclude a convulsive disorder. That a normal EEG can be recorded from a patient who has had definite clinical seizures should not be surprising, since seizures are by their very nature temporary events and may leave no clue to their presence in any examination performed between attacks. Such an intermittently active interictal abnormality may be missed unless the recording is prolonged or frequently repeated. One other consideration is the possibility that EEG abnormalities have been suppressed by anticonvulsants. If documentation of the objective abnormality is required, such medicaments may have to be withdrawn- but with caution. Furthermore, the activity usually recorded is from only the superficial cortical regions. A minimum of 18 to 21 recording electrodes is generally considered desirable for adequate coverage of even these superficial areas; occasionally more scalp electrodes may be needed to display a very small focal abnormality. Some of the activity originating from deeper areas can be recorded by special nasopharyngeal or sphenoidalleads. Exceptional circumstances may demand that recordings be made from the pial surface of the brain (electrocorticography) or from electrodes implanted into the depths of the brain (depth electrography). These last two techniques, of course, should be employed only in centers having highly specialized EEG and neurosurgical facilities.
952
DONALD
W.
KLASS
TECHNIQUES FOR ACTIVATING EEG ABNORMALITIES It is well known that EEG abnormalities often may be recorded only while the patient is asleep. If at all possible, sleep recording should be done in cases of seizure or suspected seizure, especially if the basic recording (with the patient relaxed but awake) has not provided enough distinctive diagnostic information. Less well known, perhaps, is the fact that abnormalities may appear only after sleep deprivation. 3 EEG abnormalities, and sometimes clinical seizures as well, may be evoked by other activation techniques. Two of the simplest and most useful of such techniques are hyperventilation and photic stimulation; and these are employed routinely by most electroencephalographers in examining patients with suspected seizures. Various pharmacologic agents, such as pentylenetetrazol (Metrazol), are not used routinely because they often produce discomfort and some carry a considerable risk of inducing a grand mal attack. Formerly pentylenetetrazol was administered intravenously in attempts to distinguish convulsive from nonconvulsive attacks by the threshold level at which generalized EEG abnormalities appeared. Normal subjects, as well as patients with convulsive disorders, however, show a wide range of threshold levels; so a distinction on this basis in an individual case is not reliable. 1 On the other hand, if a focal convulsive disorder is questioned, pentylenetetrazol activation may be useful, since persistent focal EEG abnormalities have not been found in records from normal persons subjected to this activation procedure. Pentylenetetrazol activation may be necessary if
RM-RE~-"v-...~..v"".,,",,",,""""'" LAP-L£~ RAP-R£~~~~~N'\I
W,hN~~~~~~~~~~--~
LPP - LE---'""'""'"'"""""'""""'""""""-'""'.J'-"'" RPP - R£~_,-v.y_~.,.-.,..j'o""""" LO-L£~~~~~~~~I~\
RO-R£~~~~~~~~II~
Looking 0/ Po/tern
~~"\a~ Looking a/ Tie in Mogazine t...!!S...J I =135 pv. Figure 2. EEG from 14-year-old patient referred because of minor seizures that had occurred after viewing patterned fabriCS, such as his father's striped neckties or checkered jackets. Paroxysmal abnormalities, as shown in tracings, could be triggered consistently by particular geometric patterns. At times they were associated with patient's typical attacks, thus exemplifying visual-pattern sensitivity.
953
THE ELECTROENCEPHALOGRAM IN THE EVALUATION OF SEIZURES
surgical excision is contemplated for the treatment of the seizures and if there has been no opportunity for adequate observation and recording during a spontaneous attack. Induction of the patient's typical seizure is essential in this situation in order (1) to observe and verify the clinical seizure pattern and (2) to substantiate the origin of the ictal discharge (which, in some cases, may be different from the location of the spontaneous interictal abnormality). The electroencephalographer will need to select the activation techniques or special procedures for the particular case, beginning with the simplest and most innocuous of them. Also, it is usually worthwhile for the electroencephalographer to search for, and attempt to reproduce, any circumstance that a patient thinks has been effective in provoking attacks in his own natural environment. In this way, important information regarding the so-called reflex epilepsies may be substantiated; and occasionally the offending environmental stimulus can be eliminated (Fig. 2).
EEG LOCALIZATION OF SEIZURE ORIGIN AND PATHOGENETIC IMPLICATIONS The clinician can determine reliably the precise site of origin and propagation route of some focal seizures from the patient's account and the character of observed attacks. In other cases, however, needed localizing information beyond that obtainable by clinical means alone may be derived from the EEG. For example, in a patient with a history of a single type of focal seizure, demonstration of multifocal electrical abnormalities suggests a type of disease which is more widespread (Fig. 3). Whereas a single focus of origin, depending on the type of abnormality, could suggest a lesion such as a primary tumor or a scar, additional widespread slow waves in the EEG might raise the question of a toxic or inflammatory disorder; independent slow-wave foci may be
/-/3~~IW~~'I~~
2-/4~~~,~~"" /3 -9
~~~~NwI,\~'Ni''''''~
/4-/0~~I~~''vV'-~''''V'i' /- 2
/3-/4~V~~1f'1~~~'1\.,,-,,·rv"'~'I~I/'oIN1" /5-/6 9-/0 ~--"w-'J'r"o.M"."'I>rl""""'"""i"'>~i'M~II-WWI/\WVWoMM"'I~IN'V~V\{>JI~"""""'~""'"""I..-J'/<"""""'M"""WV"~ ~
Figure 3.
Bilateral independent spike foci.
I' lOO!'-v.
954
DONALD
W.
KLASS
X
EYES TURNING TO RIGHT
1-3~
JERKING OF LIMBS ON RIGHT SIDe
30 SECONDS LATER. ENTIRE
SEIZURE
LASTED
4
MINUTES
Figure 4. EEG from 6-month-old child, showing multiple independent spike foci and electrographic seizure discharge which begins in right frontal region (lead 2) and spreads to adjacent regions of right hemisphere (leads 4 and 6). Clinical features alone might incorrectly have suggested origin in left hemisphere.
signs of metastatic tumors; and independent spike foci suggest multiple atrophic lesions. The clinical pattern of the seizure, especially in infants, may even be misleading for localization (Fig. 4). Frequently a situation is encountered wherein the attack, either major or minor, seems to be generalized (nonfocal) at onset. There may be no subjective aura, or at least none the patient can recall, and no objective focal motor initiation. The EEG, however, may demonstrate a focal abnormality in a region from which symptoms are not externalized directly, or a focal abnormality that becomes generalized very rapidly (Fig. 5). The possible causes of such attacks are entirely different from those of seizures truly generalized from the onset. Seizures accompanied by visceral symptoms are usually thought to originate from the temporal regions of the brain. Identical symptoms, however, may be induced by lesions in other areas, such as the orbital or mesial parasagittal regions of the frontal lobes. These symptoms seem to have a common origin within the limbic system, but can originate from locations that are widely separated. Similarly, psychic symptoms such as hallucinations during seizures are usually associated with discharges originating in the lateral superior temporal cortex;2 but these symptoms can be provoked also by lesions outside the temporal lobe, which presumably induce a temporal discharge secondarily by firing along connecting fiber pathways.4 Ictal behavior, such as automatism, may occur during a seizure involving the temporal lobe of either side of the brain. Sometimes there is no associated clinical clue, such as aphasia or a contralateral clonic motor component, to aid in determining the correct side. The EEG may provide helpfullateralizing evidence. It may also give some clue to the
955
THE ELECTROENCEPHALOGRAM IN THE EVALUATION OF SEIZURES
AGE 13 years GENERALIZED SEIZURES 2 years RIGHT LEG SMALLER THAN LEFT
2 -4 ~~-~~---' 5-7~--~~~~~1
6-8 ~~evV"~~~"'1 7-9~~~kM~~N\
8-
ION'y-V--VV-...r--..,-vv."-,,,,~"
\ ~
1= 200 l"v.
Figure 5. Note focal spike activity recorded from left parietal region (lead 7), sometimes confined to that area, sometimes initiating bursts of diffuse spike-wave complexes (left parietal spike focus with secondary bilateral synchrony). EEG indicates focal convulsive disorder even though clinical attacks apparently were generalized from onset.
cause of the attack, depending on whether unilateral or bilaterally independent foci are found. The term "petit mal" is currently used by most authorities to signify nonfocal minor seizures beginning in childhood, associated with a brief lapse of consciousness, and accompanied by a characteristic 3-persecond spike-and-wave EEG pattern (generalized and bisynchronous) during the attacks (Fig. 6). Defined in this way, petit mal seizures are rarely associated with gross structural lesions of the brain or progressive neurologic disease; and the attacks tend to decrease in response to particular types of anticonvulsant medication. Although the symptoms of brief "absence" and arrest of voluntary movement often characterize petit mal seizures, the clinical diagnosis is not always simple or certain, since similar symptoms may occur during minor seizures of focal origin also. Distinguishing minor seizures of generalized onset from those of focal origin is of great importance in the proper assessment of the cause, selection of treatment, and prognosis. Sometimes lay observers describe attacks with features suggesting
Figure 6. EEG 3 per sec spike-and-wave pattern associated with petit mal attacks (induced here by hyperventilation) in 9-year-old child.
956
DONALD
W.
KLASS
focal origin, such as jerking movements affecting mostly one side of the body. Not all unilateral clonic movements, however, represent focal seizures originating in the contralateral motor cortex. Myoclonus of subcortical origin may affect the limbs of alternate sides during different attacks. The apparent lateralization from the observation of a single attack therefore may be misleading. In this situation the EEG may be helpful by demonstrating a predominantly generalized abnormality (such as spike-wave or polyspike-wave bursts) accompanying the myoclonus without a contralateral focal rolandic abnormality.
Age and Time in EEG Interpretation Localized and persistent arrhythmic delta (less than 4 cps) waves usually indicate a recently developed or active destructive cortical lesion when recorded during the interictal period, although the changes produced by neoplasm, hemorrhage or abscess are very much alike. Focal delta activity, however, may also be a transient aftermath of a focal seizure (analogous to a clinical Todd's palsy) and does not necessarily denote a gross structural lesion. Therefore, if the initial tracing was made within about 2 days after a focal seizure, it is advisable to obtain another tracing after an additional seizure-free interval of 2 to 4 days. A persistent focal delta abnormality of equal magnitude in the second tracing would assume a more ominous significance. If the spell has not been observed and its nature is in doubt, generalized or focal abnormalities in the postictal record may help establish an organic basis for the attack, particularly if the changes no longer are present in a second record made 2 to 4 days later. Sequential EEG recordings can be helpful in other ways. An increasing focal abnormality in successive interictal tracings should GRAND MAL SEIZURES 6 YEARS RIGHT TEMPORAL ASTROCYTOMA
10-5-55
1-3
Seizures Controlled 6-5-57
~~~~~r~~~~~
2-4~~~v~
5-7~~~~"""""'''''
~~
6-8~~~~
7- 9 ~~"""f/""INvI"".~"-';(~/''V 8 -10 A./V'~.rMV'''V./V'ywJ'\{'''v(:p(¥'1~4'!'i\VW't1, L.!!£..J
I'
100
p"
Figure 7. Note irregular delta activity recorded from right temporal region (lead 14) in tracing at right, which had not been present in earlier tracing at left. Seizures, however, had been controlled by medication. EEG findings indicate progressive underlying lesion.
THE ELECTROENCEPHALOGRAM IN THE EVALUATION OF SEIZURES
957
suggest a progressive lesion such as a neoplasm or other tumor, even if the clinical seizures have been controlled by medication (Fig. 7). In the case of an adult patient with recent onset of major seizures the EEG may offer additional clues to the origin of the disorder. Rarel; does an inherited predisposition to seizures first become manifest in adult life, but the EEG may show generalized paroxysmal abnormalities to suggest this possibility. Abnormal amounts of fast (more than 13 cps) or mixed fast and slow spontaneous activity, together with paroxysmal responses to photic stimulation, raise the question of a medication withdrawal syndrome. Once again, a focal EEG abnormality would suggest an acquired structural cerebral lesion. In a group of patients with focal seizures studied at the Mayo Clinic, the additional finding of a focal abnormality of any type in the EEG more than doubled the likelihood of the presence of gross structural lesions of the brain. 6
COMMENT The foregoing examples are by no means meant to constitute an exhaustive list of the ways that the EEG may be useful in the evaluation of patients with convulsive disorders. Furthermore, the greatest usefulness for an individual patient cannot always be anticipated before the results of the EEG have been obtained. The electroencephalographer can interpret the graphic findings better if he is provided with adequate information about the specific clinical problem for which each patient is referred; and likewise, the clinician can achieve the maximal benefit for the patient by learning enough about the test so that he can select patients properly for referral and utilize the test results fully in his practice. In conclusion, let one thought be repeated: The EEG should be an integral part of the evaluation of every patient with a convulsive disorder but should never be considered the sole means of diagnosis.
REFERENCES 1. Baker, R N., and Klass, D. W.: The Metrazol activation of the normal brain. Bull Los Angeles Neurol Soc 30:201-209 (Dec.) 1965. 2. Jasper, H. H.: Functional subdivisions of the temporal region in relation to seizure patterns and subcortical connections. In Baldwin, M., and Bailey, P.: Temporal Lobe Epilepsy. Springfield, IlL, Charles C Thomas, 1958, pp. 40-57. 3. Mattson, RH., Pratt, K. L., and Calverley, J. R: Electroencephalograms of epileptics following sleep deprivation. Arch Neurol (Chicago) 13:310-315 (Sept.) 1965. 4. Schneider, R. C., Crosby, E. C., Bagchi, B. K., and Calhoun, H. D.: Temporal or occipital lobe hallucinations triggered from frontal lobe lesions. Neurology (Minneap) 11: 1 72179 (Feb.) 1961. 5. Sidell, A. D., and Daly, D. D.: Electroencephalography in epilepsy. MED CLIN N AMER 47:1541-1562 (Nov.) 1963. 6. Symposium on the clinical significance of epileptic seizures. Mayo Clin Proc 33:467-496 (Oct. 1) 1958.
Where there is much desire to learn, there of necessity will be much arguing, much writing, many opinions . ... JOHN MILTON: AREOPAGITICA
Much has been written, much has been argued, and many opinions have been expressed about the role of the electroencephalogram (EEG) in the evaluation of seizures. Indeed, we have learned a great deal since the advent of electroencephalography, as Milton might have wished. With accumulation of new information, however, opinions change; and periodic reassessment of current practice can sometimes be helpful for continued learning. In the past, considerable misunderstanding has arisen with regard to the usefulness of the EEG in diagnosis of convulsive disorders. Some clinicians have expected the test always to furnish a complete diagnosis and an outline for treatment, while others have considered it of no value whatever in the evaluation of seizures. Both viewpoints are erroneous. For comprehensive evaluation of any seizure, it is desirable to know its site of origin in the brain, the pathologic process that produces it, and the nature and mode of propagation of the electrical discharge, as well as the details of the clinical manifestations. Used properly, the EEG should be important in developing part of this knowledge. It can be regarded as an extension of the traditional neurologic examination.
EEG PATTERNS-THEIR TERMINOLOGY AND CLINICAL IMPLICATIONS When electroencephalography was first being developed, there were those who hoped that the electrical activity recorded through the intact skull and scalp would show a distinctive alteration for each type of clinical seizure, and some constant alteration to indicate the presence of a convulsive disorder between attacks. Unfortunately, these hopes have not been substantiated, for there is not a particular type of electrical abMedical Clinics of North America- Vo!. 52, No. 4, July, 1968
949
950
DONALD
W.
KLASS
NORMAL
NON SPECIFIC DYSRHYTHMIA
SPIKE AND WAVE
MULTIPLE SPIKE AND WAVE
~,~~~z SPIKE I
DELTA
!too ."."
Figure 1. Typical EEG patterns.
normality corresponding to each type of clinical attack, and between attacks the usual means of recording cannot always reveal an abnormality. The technical aspects of the EEG will not be considered here in detail, but their importance should not be underestimated. Proper recording and interpretation of the EEG require special training and extensive experience. The misinformation resulting from ignorance of the many possible technical pitfalls can be of more serious consequence than the lack of information in the absence of any test at all." Some types of interictal EEG patterns are often termed "specific" or "epileptiform," since they have a distinctive morphology and appear in a high proportion of records from patients with seizures but rarely in records from asymptomatic persons. Examples of such patterns include certain types of spikes, sharp waves, and spike-and-slow-wave complexes (Fig. 1). These patterns in the EEG allow prediction of a clinical convulsive disorder with a high degree of probability. Not all types of spikes or spike-and-wave patterns, however, have similar implications. The 14- and 6-per-second positive spikes, small sharp spikes and 6-persecond spike-and-wave complexes, for example, have a different significance (and the first two of these are considered in more detail elsewhere in this issue-see p. 941). Bursts of sinusoidal waves of abnormally slow frequency (less than 8 cycles per second) or non"'To help assess the qualifications of an electroencephalographer, the reader may wish to consult the lists of electroencephalographers certified by the Board of Qualifications of the American EEG Society, which are published in the Journal of Electroencephalography and Clinical Neurophysiology. Lists of technicians being certified by the recently formed American Board of Registration for Electroencephalographic Technologists are published in the American Journal of EEG Technology.
THE ELECTROENCEPHALOGRAM IN THE EVALUATION OF SEIZURES
951
paroxysmal aberrations of frequency are usually termed "nonspecific" (Fig. 1).5 Although these changes may appear in records from patients with seizures, they are also recorded frequently from patients with other symptoms or occasionally from asymptomatic persons; and they lack a distinctive morphology. Despite the high probability of association between some EEG patterns and clinical manifestations, the correlation is not perfect. Designation of EEG patterns by clinical terms such as "grand mal discharge" or "petit mal discharge" should be avoided, since the individual patient may have had another type of attack or-an even more disturbing discrepancy-no clinical seizures at all. Furthermore, the significance of many EEG patterns depends upon the age of the patient at the time of recording. Some types of focal spike activity, for instance, may appear transiently during childhood without overt manifestations, whereas similar activity in a record from an adult would generally have a higher correlation with clinical seizures and stable focal lesions. The relationship between particular symptoms and interictal EEG abnormalities is therefore not absolute, but rather an association of varied probability, dependent upon the nature of the symptoms and the character of the different EEG patterns. The most convincing proof of the epileptic nature of particular clinical symptoms or behavior is obtained if they occur during the EEG recording at the same time as a definite ictal EEG abnormality. This may be the only way to establish the nature of the disorder if the patient cannot or will not relate his symptoms adequately and if an attack has not been observed, or if the attack seems atypical. The absence of epileptiform discharge in a single EEG record does not exclude a convulsive disorder. That a normal EEG can be recorded from a patient who has had definite clinical seizures should not be surprising, since seizures are by their very nature temporary events and may leave no clue to their presence in any examination performed between attacks. Such an intermittently active interictal abnormality may be missed unless the recording is prolonged or frequently repeated. One other consideration is the possibility that EEG abnormalities have been suppressed by anticonvulsants. If documentation of the objective abnormality is required, such medicaments may have to be withdrawn- but with caution. Furthermore, the activity usually recorded is from only the superficial cortical regions. A minimum of 18 to 21 recording electrodes is generally considered desirable for adequate coverage of even these superficial areas; occasionally more scalp electrodes may be needed to display a very small focal abnormality. Some of the activity originating from deeper areas can be recorded by special nasopharyngeal or sphenoidalleads. Exceptional circumstances may demand that recordings be made from the pial surface of the brain (electrocorticography) or from electrodes implanted into the depths of the brain (depth electrography). These last two techniques, of course, should be employed only in centers having highly specialized EEG and neurosurgical facilities.
952
DONALD
W.
KLASS
TECHNIQUES FOR ACTIVATING EEG ABNORMALITIES It is well known that EEG abnormalities often may be recorded only while the patient is asleep. If at all possible, sleep recording should be done in cases of seizure or suspected seizure, especially if the basic recording (with the patient relaxed but awake) has not provided enough distinctive diagnostic information. Less well known, perhaps, is the fact that abnormalities may appear only after sleep deprivation. 3 EEG abnormalities, and sometimes clinical seizures as well, may be evoked by other activation techniques. Two of the simplest and most useful of such techniques are hyperventilation and photic stimulation; and these are employed routinely by most electroencephalographers in examining patients with suspected seizures. Various pharmacologic agents, such as pentylenetetrazol (Metrazol), are not used routinely because they often produce discomfort and some carry a considerable risk of inducing a grand mal attack. Formerly pentylenetetrazol was administered intravenously in attempts to distinguish convulsive from nonconvulsive attacks by the threshold level at which generalized EEG abnormalities appeared. Normal subjects, as well as patients with convulsive disorders, however, show a wide range of threshold levels; so a distinction on this basis in an individual case is not reliable. 1 On the other hand, if a focal convulsive disorder is questioned, pentylenetetrazol activation may be useful, since persistent focal EEG abnormalities have not been found in records from normal persons subjected to this activation procedure. Pentylenetetrazol activation may be necessary if
RM-RE~-"v-...~..v"".,,",,",,""""'" LAP-L£~ RAP-R£~~~~~N'\I
W,hN~~~~~~~~~~--~
LPP - LE---'""'""'"'"""""'""""'""""""-'""'.J'-"'" RPP - R£~_,-v.y_~.,.-.,..j'o""""" LO-L£~~~~~~~~I~\
RO-R£~~~~~~~~II~
Looking 0/ Po/tern
~~"\a~ Looking a/ Tie in Mogazine t...!!S...J I =135 pv. Figure 2. EEG from 14-year-old patient referred because of minor seizures that had occurred after viewing patterned fabriCS, such as his father's striped neckties or checkered jackets. Paroxysmal abnormalities, as shown in tracings, could be triggered consistently by particular geometric patterns. At times they were associated with patient's typical attacks, thus exemplifying visual-pattern sensitivity.
953
THE ELECTROENCEPHALOGRAM IN THE EVALUATION OF SEIZURES
surgical excision is contemplated for the treatment of the seizures and if there has been no opportunity for adequate observation and recording during a spontaneous attack. Induction of the patient's typical seizure is essential in this situation in order (1) to observe and verify the clinical seizure pattern and (2) to substantiate the origin of the ictal discharge (which, in some cases, may be different from the location of the spontaneous interictal abnormality). The electroencephalographer will need to select the activation techniques or special procedures for the particular case, beginning with the simplest and most innocuous of them. Also, it is usually worthwhile for the electroencephalographer to search for, and attempt to reproduce, any circumstance that a patient thinks has been effective in provoking attacks in his own natural environment. In this way, important information regarding the so-called reflex epilepsies may be substantiated; and occasionally the offending environmental stimulus can be eliminated (Fig. 2).
EEG LOCALIZATION OF SEIZURE ORIGIN AND PATHOGENETIC IMPLICATIONS The clinician can determine reliably the precise site of origin and propagation route of some focal seizures from the patient's account and the character of observed attacks. In other cases, however, needed localizing information beyond that obtainable by clinical means alone may be derived from the EEG. For example, in a patient with a history of a single type of focal seizure, demonstration of multifocal electrical abnormalities suggests a type of disease which is more widespread (Fig. 3). Whereas a single focus of origin, depending on the type of abnormality, could suggest a lesion such as a primary tumor or a scar, additional widespread slow waves in the EEG might raise the question of a toxic or inflammatory disorder; independent slow-wave foci may be
/-/3~~IW~~'I~~
2-/4~~~,~~"" /3 -9
~~~~NwI,\~'Ni''''''~
/4-/0~~I~~''vV'-~''''V'i' /- 2
/3-/4~V~~1f'1~~~'1\.,,-,,·rv"'~'I~I/'oIN1" /5-/6 9-/0 ~--"w-'J'r"o.M"."'I>rl""""'"""i"'>~i'M~II-WWI/\WVWoMM"'I~IN'V~V\{>JI~"""""'~""'"""I..-J'/<"""""'M"""WV"~ ~
Figure 3.
Bilateral independent spike foci.
I' lOO!'-v.
954
DONALD
W.
KLASS
X
EYES TURNING TO RIGHT
1-3~
JERKING OF LIMBS ON RIGHT SIDe
30 SECONDS LATER. ENTIRE
SEIZURE
LASTED
4
MINUTES
Figure 4. EEG from 6-month-old child, showing multiple independent spike foci and electrographic seizure discharge which begins in right frontal region (lead 2) and spreads to adjacent regions of right hemisphere (leads 4 and 6). Clinical features alone might incorrectly have suggested origin in left hemisphere.
signs of metastatic tumors; and independent spike foci suggest multiple atrophic lesions. The clinical pattern of the seizure, especially in infants, may even be misleading for localization (Fig. 4). Frequently a situation is encountered wherein the attack, either major or minor, seems to be generalized (nonfocal) at onset. There may be no subjective aura, or at least none the patient can recall, and no objective focal motor initiation. The EEG, however, may demonstrate a focal abnormality in a region from which symptoms are not externalized directly, or a focal abnormality that becomes generalized very rapidly (Fig. 5). The possible causes of such attacks are entirely different from those of seizures truly generalized from the onset. Seizures accompanied by visceral symptoms are usually thought to originate from the temporal regions of the brain. Identical symptoms, however, may be induced by lesions in other areas, such as the orbital or mesial parasagittal regions of the frontal lobes. These symptoms seem to have a common origin within the limbic system, but can originate from locations that are widely separated. Similarly, psychic symptoms such as hallucinations during seizures are usually associated with discharges originating in the lateral superior temporal cortex;2 but these symptoms can be provoked also by lesions outside the temporal lobe, which presumably induce a temporal discharge secondarily by firing along connecting fiber pathways.4 Ictal behavior, such as automatism, may occur during a seizure involving the temporal lobe of either side of the brain. Sometimes there is no associated clinical clue, such as aphasia or a contralateral clonic motor component, to aid in determining the correct side. The EEG may provide helpfullateralizing evidence. It may also give some clue to the
955
THE ELECTROENCEPHALOGRAM IN THE EVALUATION OF SEIZURES
AGE 13 years GENERALIZED SEIZURES 2 years RIGHT LEG SMALLER THAN LEFT
2 -4 ~~-~~---' 5-7~--~~~~~1
6-8 ~~evV"~~~"'1 7-9~~~kM~~N\
8-
ION'y-V--VV-...r--..,-vv."-,,,,~"
\ ~
1= 200 l"v.
Figure 5. Note focal spike activity recorded from left parietal region (lead 7), sometimes confined to that area, sometimes initiating bursts of diffuse spike-wave complexes (left parietal spike focus with secondary bilateral synchrony). EEG indicates focal convulsive disorder even though clinical attacks apparently were generalized from onset.
cause of the attack, depending on whether unilateral or bilaterally independent foci are found. The term "petit mal" is currently used by most authorities to signify nonfocal minor seizures beginning in childhood, associated with a brief lapse of consciousness, and accompanied by a characteristic 3-persecond spike-and-wave EEG pattern (generalized and bisynchronous) during the attacks (Fig. 6). Defined in this way, petit mal seizures are rarely associated with gross structural lesions of the brain or progressive neurologic disease; and the attacks tend to decrease in response to particular types of anticonvulsant medication. Although the symptoms of brief "absence" and arrest of voluntary movement often characterize petit mal seizures, the clinical diagnosis is not always simple or certain, since similar symptoms may occur during minor seizures of focal origin also. Distinguishing minor seizures of generalized onset from those of focal origin is of great importance in the proper assessment of the cause, selection of treatment, and prognosis. Sometimes lay observers describe attacks with features suggesting
Figure 6. EEG 3 per sec spike-and-wave pattern associated with petit mal attacks (induced here by hyperventilation) in 9-year-old child.
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focal origin, such as jerking movements affecting mostly one side of the body. Not all unilateral clonic movements, however, represent focal seizures originating in the contralateral motor cortex. Myoclonus of subcortical origin may affect the limbs of alternate sides during different attacks. The apparent lateralization from the observation of a single attack therefore may be misleading. In this situation the EEG may be helpful by demonstrating a predominantly generalized abnormality (such as spike-wave or polyspike-wave bursts) accompanying the myoclonus without a contralateral focal rolandic abnormality.
Age and Time in EEG Interpretation Localized and persistent arrhythmic delta (less than 4 cps) waves usually indicate a recently developed or active destructive cortical lesion when recorded during the interictal period, although the changes produced by neoplasm, hemorrhage or abscess are very much alike. Focal delta activity, however, may also be a transient aftermath of a focal seizure (analogous to a clinical Todd's palsy) and does not necessarily denote a gross structural lesion. Therefore, if the initial tracing was made within about 2 days after a focal seizure, it is advisable to obtain another tracing after an additional seizure-free interval of 2 to 4 days. A persistent focal delta abnormality of equal magnitude in the second tracing would assume a more ominous significance. If the spell has not been observed and its nature is in doubt, generalized or focal abnormalities in the postictal record may help establish an organic basis for the attack, particularly if the changes no longer are present in a second record made 2 to 4 days later. Sequential EEG recordings can be helpful in other ways. An increasing focal abnormality in successive interictal tracings should GRAND MAL SEIZURES 6 YEARS RIGHT TEMPORAL ASTROCYTOMA
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Figure 7. Note irregular delta activity recorded from right temporal region (lead 14) in tracing at right, which had not been present in earlier tracing at left. Seizures, however, had been controlled by medication. EEG findings indicate progressive underlying lesion.
THE ELECTROENCEPHALOGRAM IN THE EVALUATION OF SEIZURES
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suggest a progressive lesion such as a neoplasm or other tumor, even if the clinical seizures have been controlled by medication (Fig. 7). In the case of an adult patient with recent onset of major seizures the EEG may offer additional clues to the origin of the disorder. Rarel; does an inherited predisposition to seizures first become manifest in adult life, but the EEG may show generalized paroxysmal abnormalities to suggest this possibility. Abnormal amounts of fast (more than 13 cps) or mixed fast and slow spontaneous activity, together with paroxysmal responses to photic stimulation, raise the question of a medication withdrawal syndrome. Once again, a focal EEG abnormality would suggest an acquired structural cerebral lesion. In a group of patients with focal seizures studied at the Mayo Clinic, the additional finding of a focal abnormality of any type in the EEG more than doubled the likelihood of the presence of gross structural lesions of the brain. 6
COMMENT The foregoing examples are by no means meant to constitute an exhaustive list of the ways that the EEG may be useful in the evaluation of patients with convulsive disorders. Furthermore, the greatest usefulness for an individual patient cannot always be anticipated before the results of the EEG have been obtained. The electroencephalographer can interpret the graphic findings better if he is provided with adequate information about the specific clinical problem for which each patient is referred; and likewise, the clinician can achieve the maximal benefit for the patient by learning enough about the test so that he can select patients properly for referral and utilize the test results fully in his practice. In conclusion, let one thought be repeated: The EEG should be an integral part of the evaluation of every patient with a convulsive disorder but should never be considered the sole means of diagnosis.
REFERENCES 1. Baker, R N., and Klass, D. W.: The Metrazol activation of the normal brain. Bull Los Angeles Neurol Soc 30:201-209 (Dec.) 1965. 2. Jasper, H. H.: Functional subdivisions of the temporal region in relation to seizure patterns and subcortical connections. In Baldwin, M., and Bailey, P.: Temporal Lobe Epilepsy. Springfield, IlL, Charles C Thomas, 1958, pp. 40-57. 3. Mattson, RH., Pratt, K. L., and Calverley, J. R: Electroencephalograms of epileptics following sleep deprivation. Arch Neurol (Chicago) 13:310-315 (Sept.) 1965. 4. Schneider, R. C., Crosby, E. C., Bagchi, B. K., and Calhoun, H. D.: Temporal or occipital lobe hallucinations triggered from frontal lobe lesions. Neurology (Minneap) 11: 1 72179 (Feb.) 1961. 5. Sidell, A. D., and Daly, D. D.: Electroencephalography in epilepsy. MED CLIN N AMER 47:1541-1562 (Nov.) 1963. 6. Symposium on the clinical significance of epileptic seizures. Mayo Clin Proc 33:467-496 (Oct. 1) 1958.