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Detection of epileptiform activity by different noninvasive EEG methods in complex partial epilepsy.

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to improve muscle strength 1111, and lactate, another
potential chelator of calcium ions, was shown to aggravate myasthenic weakness 112).
Changes in total and ionized serum calcium concentrations during plasmapheresis result from two
sources: the use of ACD for anticoagulation and the
replacement of plasma by calcium-poor albumin solution. Plasmapheresis reduces total and ionized calcium
concentration by 15 to 20% [13-15}, and when only
ACD is infused without plasma removal, a decrease in
[Ca*+J of up to 33% may occur [13]. These changes in
calcium levels produce mild or no symptoms in nonmyasthenic patients. Transient worsening of myasthenic weakness during plasmapheresis has been previously reported 1163, but its association with calcium
levels has not been discussed.
It seems reasonable to state that some myasthenic
patients may be highly sensitive to citrate-induced decreases in [Ca2+]. This fact may justify an effort to
monitor ionized calcium levels and to supplement calcium vigorously during plasmapheresis, as has been
our practice recently.
This work was supported in part by the Reichmann Foundation and
the Nina Silverman Memorial Fund.
Presented in part at the First Meeting of the European Neurological
Society, Nice, France, June 22, 1988. An abstract has been published (J Neurol 1988;235[Suppl 1):S80).
References
1. Consensus Conference. The utility of therapeutic plasmapheresis for neurological disorders. JAMA 1986;256:1333-1337
2. Hazards of apheresis. Lancet 1982;2:1025-1026
3. Rodnitzki RL, Goeker JA. Complications of plasma exchange in
neurological patients. Arch Neurol 1982;39:350-354
4. Thorlacius S, Aarli JA, Jakobsen H , Halvorsen K. Plasma exchange in myasthenia gravis, clinical effect. Acta Neurol Scand
1985;72 :464-468
5. Aids to the examination of the peripheral nervous system. London: Bailliere Tindall, 1986:l
6. Argov 2, Brenner T, Abramsky 0. Ampicillin may agravate
clinical and experimental myasthenia gravis. Arch Neurol
1986;43:255-256
7. Brenner T, Abramsky 0,Lisak RP, et al. Radioimmunoassay of
antibodies to acetylcholine receptor in serum of myasthenia
gravis patients. Isr J Med Sci 1978;14:986-987
8. Ceccarelli B, Hurlbut WP. Vesicle hypothesis of the release of
quanta of acetylcholine. Physiol Rev 1980;60:396-44 1
9. Swift TR, Greenberg MK. Miscellaneous neuromuscular transmission disorders. In: Brumback RA, Gerst JN, eds. The neuromuscular junction. Mount Kisco, N Y Futura, 1984:295-324
10. McQuillen MP, Cantor HE, ORourke JR. Myasthenic syndrome associated with antibiotics. Arch Neurol 1968;18:402415
11. Kornfield P, Somlyo A, Osserman KE. Role of calcium in myasthenia gravis. Arch Neurol 1969;2 1:466-470
12. Patten BM, Oliver KL, Engel WK. Effect of lactate infusion on
patients with myasthenia gravis. Neurology 1974;24:986-990
13. Silberstein LE, Naryshkin S, Hadad JJ, Strauss JF. Calcium homeostasis during therapeutic plasma exchange. Transfusion
1986;26:15 1-155
14. Watson DK, Penny AF, Marshall RW, Robinson AE. Citrate
induced hypocalcemia during cell separation. Br J Haematol
1980;44:503-507
15. Buskard NA, Varghese 2, Wills MR. Correction of hypocalcemic symptoms during plasma exchange. Lancet 1976;2:344345
16. k s a k RP, Abramsky 0, Schotland D. Plasmapheresis in the
treatment of myasthenia gravis: preliminary studies in 2 1 patients. In: Dau PC, ed. Plasmapheresis and the immunobiology
of myasthenia gravis. Boston: Houghton-Mifflin, 1979:209215
Detection of Epileptiform
Activity by Different
Noninvasive EEG
Methods in Complex
Partial Epilepsy
Douglas S. Goodin, MD, Michael J. Aminoff, MD, FRCP,
and Kenneth D. Laxer, MD
The diagnostic utility of different noninvasive electrode
placements for deriving the electroencephalogram and
detecting interictal epileptiform discharges was compared. Anterior temporal and nasopharyngeal electrodes in combination with routine scalp electrodes detected over 97% of the spikes, whereas recording from
only standard electrode placements detected 58%.
Minisphenoidal and surface sphenoidal electrodes were
generally not helpful. I n some circumstances, however,
the use of surface sphenoidal electrodes provided important confirmatory information. In no case did the minisphenoidal electrodes provide unique information, and
their use seems unjustified, although the inclusion of
other nonstandard electrodes in the recording montage
is important to increase the yield.
Goodin DS, Aminoff MJ, Laxer KD. Detection of
epileptiform activity by different noninvasive
EEG methods in complex partial epilepsy.
Ann Neurol 1990;27:330-3 34
In a number of patients with clinically unequivocal
complex partial seizures, the electroencephalogram
(EEG) recorded from conventionally placed electrodes
From the Department of Neurology, University of California, San
Francisco, School of Medicine, San Francisco, CA.
Received Jun 14, 1989, and in revised form Sep 6. Accepted for
publication Sep 10, 1989.
Address correspondence to Dr Goodin, Department of Neurology,
M-794, University of California, San Francisco, San Francisco, CA
94143-0114.
330 Copyright 0 1990 by the American Neurological Association
fails to reveal any interictal abnormalities. The presence of such abnormalities is important, however, both
for confirming the clinical diagnosis and, in some instances, for aiding in the determination of the feasibility of operative treatment. For this reason, attempts
have been made to improve the diagnostic yield of the
EEG by recording from specially placed, noninvasive
additional electrodes. Some authors have suggested
that anterior temporal electrodes are the most useful
11, 2) of these additional electrodes, whereas others
have advocated nasopharyngeal electrodes 131, surface
sphenoidal electrodes 141, or minisphenoidal electrodes { 51. This latter technique, however, requires the
insertion of needles through the surface of the skin
and, if it is to be used routinely, should provide information complementary to that obtained from the other
recording derivations. We are not aware of any published study that has compared the diagnostic utility of
all these recording derivations. We therefore prospectively determined the value of each of these recording
derivations, both alone and in combination, in detecting interictal epileptiform activity in the EEG of patients with complex partial seizures.
Methods
We studied 50 patients with known or suspected complex
partial seizures (aged 18-72 years) who were referred to our
EEG laboratory and in whom we were requested to use one
or another of these special recording derivations. The special
recording arrangements were generally requested either in
the belief that they would increase the likelihood of detecting epileptiform abnormalities in patients with no abnormalities on routine EEG, or in the hope that they would permit
better localization of an epileptogenic focus. In each patient,
after the routine EEG an additional bipolar montage was run
during the same recording session, incorporating all of the
special electrode placements. This montage was run for 5
minutes while the patient was either awake or asleep.
Anterior temporal electrodes (T1 and T2) were placed 1
cm above and one-third the distance along the line from the
external auditory meatus to the external canthus of the eye
[6]. Nasopharyngeal electrodes (NP1 and NP2) were placed
bilaterally and secured with micropore tape [7]. Minisphenoidal electrodes (MS1 and MS2) were placed 2 cm anterior
to the tragus just below the zygomatic arch. The electrode
was inserted to the hub, perpendicular to the skin surface,
and secured with micropore tape. Surface sphenoidal electrodes (SS1 and SS2) were placed 1 cm anterior to the tragus
and in the same axial plane as the minisphenoidal electrodes.
The remaining electrodes were placed over the scalp according to the international 10-20 system.
The 21 channels of the bipolar recording montage consisted of Fpl-F7, F7-T3, T3-T5, Fp2-F8, F8-T4, T4-T6, C3T3, T3-NP1, NP1-NP2, NP2-T4, T4-C4, T3-MS1, MS1MS2, MS2-T4, T3-SS1, SS1-SS2, SS2-T4, T3-T1, Tl-T2,
T2-T4, and EKG. The derivations involving the special electrode placements are ones commonly favored by electroencephalographers. One possible bias of our analysis is that the
interelectrode distances varied depending on the recording
derivation. Depending on the precise site of origin of individual spike discharges, however, this bias may favor one or
another of the various recording derivations that we employed. We did not use a referential montage because of
difficulty in selecting a suitable inactive reference point and
because many authorities prefer bipolar recordings for the
localization of sharp transients.
Each record was interpreted by two board-certified electroencephalographers (D. S. G. and M. J. A.) and only spikes
or sharp waves agreed on by the two were included in the
analysis. The presence or absence of spikes or sharp waves in
each of the recording channels connected with the special
recording sites was judged independently of the findings in
other channels. A sharp wave or spike was judged as unequivocal and abnormal if it had a sharp contour, a duration
of less than 200 msec, and was clearly distinct from the
ongoing background activity by its amplitude and duration.
Such discharges were usually asymmetrical in appearance and
were often followed by a slow wave [ S ] .
Results
Of the 50 patients evaluated, 30 (10 male, 20 female;
mean age, 37.1 years) had no spikes or sharp waves
detected during the 5 minutes of recording using the
special montage. In the remaining 20 patients (6 male,
14 female; mean age, 31.4 years), between 1 and 107
spikes or sharp waves were seen during this recording
period. A total of 529 spikes were seen in these 20
patients (mean, 26.5 spikedpatient). In 1 patient brief
(less than 1 second) bursts of polyspike activity were
seen in addition to isolated spikes and, for the purposes of this analysis, each burst was considered as a
single spike. The percentages of spikes detected by
each special electrode placement both individually and
in combination with other placements are listed in
Table 1. The electrode placement most likely to detect
spikes was the anterior temporal electrode, which
alone detected 70% of the epileptiform discharges.
The nasopharyngeal electrodes were the least likely to
detect abnormalities, with only 56% of the spikes detected by these electrodes. This was partly due to the
fact that in 4 subjects the recording from the nasopharyngeal electrodes was almost completely obscured by
artifact (Table 2). Despite this, however, the nasopharyngeal electrode contributed important additional information. Thus, 13% of the spikes seen were detected only by the nasopharyngeal electrodes and 1
patient had spikes seen only in this derivation (Figure;
see Table 2). The combination of anterior temporal
electrodes and nasopharyngeal electrodes detected
86% of the observed spikes and when these were both
added to the standard electrode placements, more than
97% of the spikes were detected (see Table 1).
By contrast, the minisphenoidal and surface sphenoidal electrodes contributed very little to spike detection. Taken together, only 2.6% of the spikes were
Brief Communication: Goodin et al: Detection of Epileptiform Activity 331
Table 1. Percentage of Spikes Detected by Derivations Involving Different
Electrode Placements, Both Individually and in Combination with Other Derivations"
Additional Electrode Placements
Primary Electrode
Placements
None
Standard
58
70
62
61
56
-
Anterior
Temporal
Surface
Sphenoidal
Minisphenoidal
~~
Standard
Anterior temporal
Minisphenoidal
Surface sphenoidal
Nasophar y ngeal
-
81
75
74
69
-
75
74
86
-
63
79
77
"When no additional electrodes are used, the numbers indicate the percent yield from only the primary electrode placement. The remaining
numbers indicate the total percent yield when the findings from both the primary and the additional electrode placements are considered. The
yield of recording from the standard electrode placements plus two additional placements was as follows: anterior temporal plus nasopharyngeal,
97%; minisphenoidal plus nasopharyngeal, 90%; surface sphenoidal plus nasopharyngeal, 89%; minisphenoidal plus anterior temporal, 86%;
surface sphenoidal plus anterior temporal, 86%; and surface sphenoidal plus minisphenoidal, 75%.
Table 2. Comparison of Diagnostic Yield and Technical Problems with Each
Recording Derivation in the 20 Subjects with Spikes in Their EEG
Electrode Placements
Variable
Standard
Placements
Anterior
Temporal
Minisphenoidal
Surface
Sphenoidal
Nasopharyngeal
Mini- and Surface
Sphenoidal
1
2
2
2
2
2
1
0
0
0
1
0
50 (9.5%)
31 (5.9%)
0 (0%)
1 (0.2%)
70 (13.2%)
14 (2.6%'0)"
0
1
0
0
4
0
~
No. of patients without
any spikes in a particular derivation
No. of patients in whom
all spikes were only in
one derivation
No. (%) of spikes seen
only in one derivation
No. of records with
technical problems in
individual derivations
~~
~
"Eleven of these spikes occurred when the anterior temporal electrode was uninterpretable because of artifact. Similar discharges were also seen
in the anterior temporal electrodes on other occasions when the artifact was absent. This suggests that in many instances the spike discharges
would have been detected by the anterior temporal placement.
seen only with these electrodes (see Table 2), and in
no case did the minisphenoidal electrodes add complementary information to that provided by the other
electrodes (see Table 2).
The presence of epileptiform activity at one location
may also be useful in confirming or clarifying an ambiguous abnormality at an adjacent site. We therefore
also examined our data to determine the usefulness of
each electrode placement in providing such confirmatory information. A confirmed spike was taken to be an
unequivocal spike seen simultaneously in two or more
locations and, for the purpose of this analysis, the
sphenoidal location was considered as the combined
yield of the minisphenoidal and surface sphenoidal
electrodes. There were 354 confirmed spikes in our
study. In 93 instances (26%) the anterior temporal
332 Annals of Neurology Vol 27 N o 3 March 1990
electrodes provided the only confirmatory information, i.e., detected spikes when these were seen at only
one of the other three locations. In 44 instances (12%)
the surface sphenoidal electrode (often with a spike
also seen in the recording from the minisphenoidal
electrodes) provided this information. In 30 instances
(8%) this confirmatory information was provided by
only the standard placements and in 27 instances (8%)
by only the nasopharyngeal electrode; in only 5 instances (1%) did the minisphenoidal electrode alone
do so.
Discussion
The results of this study indicate that there is n o single
recording montage that adequately detects all epileptiform discharges in patients with complex partial sei-
Fpl-F7
.VJ\
,-.
F7-T3
T3-T5
-
uzh,
Fp2-F8
F8-T4
?-
+
,-.
T4-T6
_yI_-
MS1-MS2
-4-L-
-
T3-MS1
kr
-J-“%,-
-
MS2-T4
T3-SS1
+
-
-
SSl-ss2
SS2-T4
--
T3-T1
-4J-
6-u-
c
T1 -T2
T2-T4
EKG
-1
EEG recordedfrom standard electrode placements as well as from
nasopharyngeal (NP), minisphenoidal (MS), su$ace sphenoidal
(SS), and anterior temporal (TI and T2) electrodes. The asteriskr indicate unequivocal spike or sharp wave didarges. The
discharge indicated by the third asterisk from the ldt was rejected at other electrode sites but was judged “definitely epilept;frm” only at the NP site; at the other locations, the discharge
was less sharp and less distinct fmm the background slow activity with which it was intermixed, The other sharp wave discharges were only seen in the NP electrodes. Additional discharges seen at the NP site were regarded as equivocal.
zures. Recordings from standard electrode placements
on the scalp detected only 58% of such discharges. In
agreement with the observation of others 11, 2) the
anterior temporal electrodes were the best, but even
these failed to detect 30% of the discharges that were
seen using other recording derivations and failed to
detect any spikes in 10% of the patients in whom
spikes were seen elsewhere (see Tables 1 and 2). The
nasopharyngeal electrodes frequently provided additional information by recording spikes that were not
seen in the other recording derivations. However, in
20% of our patients the recording made from nasopharyngeal electrodes was contaminated by artifact and
therefore uninterpretable, and several other patients
had to be excluded from our study because they would
not tolerate insertion of these electrodes. Some authors [ 3 ) have also stressed the diagnostic utility of
nasopharyngeal recordings, whereas others 121 have
emphasized the technical difficulties encountered with
these electrodes. Despite the technical difficulties,
however, recording from the nasopharyngeal and anterior temporal electrodes detected 86% of the spikes
and, if recordings were also made from standard electrodes it was possible to detect over 97% of these
epileptiform discharges in our experience.
By comparison, the surface sphenoidal and minisphenoidal electrodes provided relatively little complementary information and in no case was the epileptiform discharge confined to the minisphenoidal
electrodes. Laxer 15) originally suggested that the routine use of minisphenoidal electrodes might help in the
evaluation of patients with known or suspected epilepsy, but his study did not compare the usefulness of
recordings from surface sphenoidal and minisphenoidal electrodes or, in fact, the comparative utility of any
of the nonstandard electrodes that we studied. Our
findings thus suggest that the routine use of minisphenoidal electrodes is not justified since other electrodes
can provide the same information.
In conclusion, the routine noninvasive electrophysiological evaluation of patients with known or suspected complex partial seizures should include both
nasopharyngeal and anterior temporal electrodes in addition to the routine scalp montage, if the chances of
Brief Communication: Goodin et al: Detection of Epileptiform Activity 333
detecting interictal epileptiform activity are to be maximized. Noninvasive recordings from the sphenoidal
region may be justified in selected patients but this
does not require the use of minisphenoidal electrodes.
Addendum
Since the submission of our paper for publication, Sadler and
Goodwin [9} have reported a study similar to ours to determine the relative sensitivity of different electrode placements
for detecting spike discharges in patients with complex partial seizures. However, their data are presented in such a way
that direct comparison with our findings is difficult, and it is
not possible to determine whether the combination of electrodes that we found most useful was similarly helpful in
their experience. From personal communication with these
authors, however, we can comment further about their experience with nasopharyngeal electrodes. Among the patients
in their series in whom recordings were made from nasopharyngeal electrodes, a total of 159 spikes were detected but
only 2 (1.3%) of these were seen exclusively in the nasopharyngeal electrodes. The reason for such a low yield probably
relates in part to selection factors. Thus, we studied a group
of unselected patients with complex partial seizures whereas
Sadler and Goodwin intentionally selected patients who
were known from previous EEG studies to have spike discharges in the lateral anterior temporal region.
References
1. Homan RW, Jones MC, Rawat S. Anterior temporal electrodes
in complex partial seizures. Electroencephalogr Clin Neurophysiol 1988;70:105-109
2. Sperling MR, Engel J Jr. Electroencephalographic recording from
the temporal lobes: a comparison of ear, anterior temporal, and
nasopharyngeal electrodes. Ann Neurol 1985;17:510-513
3. Levin R, Leaton EM, Lee SI. The value of nasopharyngeal recording in psychiatric patients. Biol Psychiatry 1986;21:1236-1238
4. Sadler M, Goodwin J. The sensitivity of various electrodes in the
detection of epileptiform potentials (EPs) in patients with partial
complex (PC) seizures. Epilepsia 1986;27:627 (Abstract)
5. Laxer KD. Mini-sphenoidal electrodes in the investigation of seizures. Electroencephalogr Clin Neurophysiol 1984;58:127-129
6. Silverman D. The anterior temporal electrode and the ten-twenty
system. Electroencephalogr Clin Neurophysiol 1960;12:735737
7. Mavor H, Hellen MK. Nasopharyngeal electrode recording. Am
J Electroencephalogr Tech 1964;4:43-50
8. Gloor P. Contributions of electroencephalography and electrocorticography to the neurosurgical treatment of the epilepsies.
Adv Neurol 1975;8:59-105
9. Sadler RM, Goodwin J. Multiple electrodes for detecting spikes
in partial complex seizures. Can J Neurol Sci 1989;16:326-329
Evelid Twitching Seizures
and GenerahzedY
Tonic-Clonic Convulsions:
A Syndrome of Idiopathic
Generahzed Epilepsy
John W. Miller, MD, PhD,*
and James A. Ferrendelli, MD*I
This is a report of two neurologically normal patients
who had primary generalized seizures consisting of irregular fluttering or twitching movements of the eyelids
accompanied by generalized, rhythmic 9- to 15-H~electroencephalographic discharges as well as infrequent
generalized tonic-clonic seizures. This is a syndrome of
idiopathic generalized epilepsy that responds to treatment with valproic acid.
Miller JW,
Ferrendelli JA. Eyelid twitching
seizures and generalized tonic-clonic convulsions:
a syndrome of idiopathic generalized epilepsy.
Ann Neurol 1990;27:334-336
Various eyelid movements are known to occur during
seizures. Myoclonic twitches or closure of the upper
lids are a well-recognized correlate to absence seizures
with generalized spike and wave discharges El-41. A
less-discussed phenomenon is eyelid twitching o r myoclonus with a generalized, rhythmic, rapid electroencephalographic (EEG) discharge. We describe 2 patients with this type of seizure.
Case Reports
Patient 1
A woman was first seen on May 4, 1987 at the age of 39
years. At age 16 she had her first generalized tonic-clonic
convulsion. Subsequently she had six more convulsions. All
were similar; they often were preceded by sleep deprivation
or occurred during pregnancy. For a few hours or even days
prior to each convulsion she had numerous brief episodes of
eyelid twitching. She was intially treated with phenobarbital,
and subsequently acetazolamide and phenytoin without seizure control. A cranial computed tomographic (CT) scan in
1981 was normal.
When seen, the patient was taking phenytoin, 200 mg
twice daily; phenobarbital, 60 mg twice daily; and acetazolamide, 250 mdday. She was the product of a normal labor
and delivery and denied any family history of seizures (she
has two sisters and one child) or any history of head trauma
From the 'Department of Neurology and Neurological Surgery
(Neurology) and the tDeparunent of Pharmacology, Washington
University School of Medicine, St. Louis, MO.
Received Jul 20, 1989. Accepted for publication Sep 12, 1989.
Address correspondence to Dr Miller, Department of Neurology,
Washington University School of Medicine, 660 South Euclid, St.
Louis. MO 631 10.
334
Copyright 0 1990 by the American Neurological Association
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