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Depth electroencephalography in selection of refractory epilepsy for surgery.

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Depth Electroencephalography
in Selection of Refractory Epilepsy for Surgery
Sfisan Soloway Spencer, M D
Depth electroencephalography (EEG) is sometimes used t o evaluate medically refractory epileptic patients for surgical treatment. Surgical excision of well-defined epileptogenic foci has been shown repeatedly to cause a substantial reduction of seizure frequency in 60 to 80% of these patients; however, because surgical success is no better at
centers that employ depth EEG in patient evaluation, the procedure remains controversial. Review of the available
literature shows that depth EEG results reported to date, when compared to scalp EEG results in 178 patients, could
have enabled selection of 36% more patients for surgery by defining otherwise unidentifiable single epileptogenic
foci. Furthermore, depth EEG could have prevented surgery in another 18% by demonstrating different or additional epileptogenic foci in patients otherwise thought to have a single discharging focus amenable t o resection.
Thus depth EEG had the potential to alter the surgical decision in more than 50% of patients reported. Centers that
employ depth EEG may evaluate a different population of patients, which could account for their lack of increased
surgical success.
Spencer SS: Depth electroencephalography in selection of refractory epilepsy for surgery.
Ann Neurol 9:207-214, 1981
Epidemiological and Etiological Factors
Epilepsy affects at least 1 in 200 Americans [ 11, 541.
For every patient with generalized epilepsy, at least 2
suffer with partial epilepsy [ 3 7 ] .Thus, of the population of more than 1 million epileptics in the IJnited
States, upward of 600,000 have partial seizures.
Since detailed studies indicate failure of seizure control in 30% or more of epileptic patients [641, there
are about 200,000 patients with uncontrolled partial
epilepsy in this country. The number who might be
helped by excision of an epileptogenic focus has been
variously cited as 45,000 to 100,000 Ell, 14, 541.
Experimental data provide impetus in the search
for methods of seizure control. The phenomenon of
experimental kindling, whereby repetitive electrical
stimuli to the brain result in spontaneous seizure activity following cessation of stimulation [ 2 5 , 2 6 , 301
suggests that repetitive spontaneous discharges of
epileptic foci in humans and the continual exposure
of normal neuronal pools to this paroxysmal activity
may similarly induce seizures in these normal pools.
How susceptible certain areas of human brain are to
such conditions is not established. The possibility
exists that permanent transsynaptic changes can
occur, locally or at a distance, and they may be of
sufficient magnitude to result in modification of seizure threshold o r even in the creation of new foci of
spontaneous seizure discharge. This concept has implications in terms of duration of seizures and the
need for operative therapy in intractable cases. N o t
only might earlier intervention be indicated, but
techniques for reliable identification of multiple independent foci of paroxysmal activity become essen-
From the Department of Neurology, Yale University School of
Medicine, 333 Cedar St, New Haven, CT 06510.
Received Dec 13, 1979, and in revised form July 25 and Oct 17,
1980. Accepted for publication Oct 18, 1980.
Despite recent advances in treatment, including the
introduction of several new anticonvulsant drugs in
the past decade and refinement of techniques for
determining serum anticonvulsant levels, epilepsy
remains a major health problem. Repeated studies
have shown that surgical excision of an epileptogenic
focus reduces o r abolishes seizures in 60 to 80% of
selected patients with medically refractory focal epilepsy [ 5 , 7 , 14, 17,35,36,41,42,58,60,70,731, but
ways to decrease the surgical failure rate and to increase utilization of this form of treatment have yet
to be established. Depth electroencephalography
(EEG) has been promoted by some centers as a diagnostic procedure with the potential for improving
selection of medically refractory epileptics for surgery. Because of the risks and costs involved and the
lack of clearly established benefit, its used continues
to be a source of controversy. Although further
studies may be needed, considerable data already
exist in the literature.
Address reprint requests to Dr Spencer.
0364-5134/8l/030207-08$01.25 @ 1980 by the American Neurological Association 207
compared to the less than 50% success rate in patients with partial temporal lobe excision (right, 4.5
cm; left, 3.9 cm). These authors emphasized that removal of less than the entire epileptogenic cortex,
which may be quite large, contributes to surgical failures [50]. Rasmussen et a1 [60] showed increased
surgical success with temporal and occipital lobe resections (61 to 71%) as compared with frontal and
parietal lobe resections (59 to 62%); frontal and
parietal resections of large epileptogenic areas are
more likely to be limited by considerations about the
acceptable neurological deficit. Jasper and Rasmussen [401 and Rasmussen [59] noted, however, that
removal of the bulk, and not necessarily the entirety, of epileptogenic tissue may be sufficient for a
good result. (5) Surgical success rates are better with
a unilateral focus than with bilateral epileptogenic
foci. Penfield and Flanigin [56] showed 64% success
in patients with unilateral epileptic abnormalities versus 20% success in patients with bilateral shifting
foci; Bloom et a1 [71 had similar results, with 65%
versus 25% success in the two groups. Bailey and
Gibbs [3], van Buren et a1 [72], and Green and
coworkers [32, 341 also reported a decline in surgical success with decreased EEG localization of
the epileptic abnormality. The studies document a
gradual improvement in surgical success rate as the
amount of bilateral abnormality decreases. The results of Olivier et al [55] are consistent in that patients with more than SO% of their seizures arising in
a single epileptic focus had a good surgical outcome.
Since patients with multiple epileptogenic foci are
poor surgical candidates, reliable means of detecting
such foci would minimize nonindicated operations
and improve surgical success. Conversely, measures
that could reliably detect unifocal disease would increase the possibility of surgical treatment for medically refractory cases. Quantification of the degree of
bilateral abnormality may also be important in improving surgical success.
Localization of E E G Foci
The reliable localization of epileptogenic cerebral tissue continues to be a controversial issue [76]. Most
centers consider a patient a candidate for surgery
if recurrent seizures interfere extensively with life, if
the seizures cannot be controlled adequately despite
therapeutic trials of all appropriate anticonvulsant
drugs, and if focal epilepsy is a diagnostic possibility
[33, 52, 611. The approach to further localization
differs. Neuroradiological procedures usually can
identify mass lesions, removal of which produces a
high rate of seizure remission [17, 221. But most
often such abnormalities are absent. The use of positron emission tomography to identify areas of brain
hypofunction has recently been promoted as a
superior method for localization [ 2 3 ] ,but more data
are needed. Measuring regional cerebral blood flow
is being investigated to localize epileptogenic foci,
but the technique is still not fully developed [38].
Scalp EEG with supplementary proceduresincluding overnight recording and sphenoidal and
nasopharyngeal leads-has
been the traditional
means of localization and the one upon which most
studies in Table 1 were based. The direct recording
of spontaneous seizures from the scalp is often insufficient to localize or even lateralize seizure onset,
however, and more reliance is then placed on interic tal abnormalities. Electrocorticography, although
still used widely [29], suffers from the disadvantages of limited time for recording, usually without
ictal events, and from the restricted area of accessibility [4]. A method for continuous recording of
cortical regions by implantation of epidural Silastic
sheets described recently by Goldring [31] may
prove to be a major advance in evaluation of certain
epileptic patients, because it enables sufficient time
for possible ictal recording. The technique has the
disadvantages that a craniotomy is needed and that the
locale for investigation must be selected preoperatively. Electrical stimulation and chemical seizure induction have poor reliability for localization when
compared to spontaneous seizures [77].
Some epileptologists believe that direct recording
of the onset and discharge of seizures from the
depths of the brain using implanted intracerebral
electrodes provides the best possible evidence of a
focus [29, 51, 65, 75, 761.
Depth EEG
Talairach et a1 [ l o , 69-71] pioneered depth recording of the EEG for localization prior to surgery in
focal epilepsy. Use of the technique remains confined
to a handful of epilepsy centers with the appropriate
facilities, equipment, and staff. The duration of recording can vary from several hours (as in intraoperative recording, the so-called acute depth
EEG) to several weeks, during which the EEG may
be monitored intermittently or continuously, with or
without telemetry. Various systems are in use for
storage of EEG information on paper or magnetic
tape. Some centers store only the graphs of seizures
for later detailed review. O ne can select different
montages for simultaneous recording of the scalp
and depth EEG, with or without sphenoidal or
nasopharyngeal leads, depending on the sites of
maximal abnormality on screening determinations.
Depth recording requires a highly trained staff capable of interpreting the EEG records, evaluating patients during seizures, and operating all necessary
equipment. Facilities for construction, repair, and
maintenance of the electrodes are desirable.
Neurological Progress: Spencer: Depth Electroencephalography 209
Table I . Representative Surgical Results in Focal Refractory Epilepsy
Tot a1
Patient Povulation
Bhatia and Kollevold [51,
Focal intractable epilepsy, including tumors without raised intracranial pressure
Temporal lobe epilepsy with bilateral foci
Both sides equal
One side predominant
Temporal lobe epilepsy, with or
without other seizure types
Children with temporal lobe epilepsy
Mesial temporal sclerosis
Nonspecific lesions
Temporal lobe epilepsy, including
patients with tumors
Focal intractable epilepsy
Bloom et a1 [71, 1960
Crandall [14], 1975
Davidson and Falconer [ 171,
Green and Scheetz [35],
Greenwood and Kellaway
[361, 1969
Jensen and Vaernet [441,
Penfield and Flanigm [56],
1950 (see also Jasper et a1
Rapport et a1 [581, 1977
Rasmussen [601, 1975
Talairach and Bancaud 1701,
Van Buren et a1 [731, 1975
Wieser et a1 [771, 1979
7 1%
Temporal lobe epilepsy
Temporal lobe epilepsy
Bilateral synchronous EEG
Bilateral independent EEG
Unilateral EEG
Focal intractable epilepsy
Focal intractable epilepsy
Birth trauma
Pos ttraumatic
Abnormality not known
Temporal lobe
Occipital lobe
Parietal lobe
Frontal lobe
Temporal lobe epilepsy
In 12
Temporal lobe epilepsy
Total resection
Partial resection
Temporal lobe epilepsy
With spontaneous seizures
Without svontaneous seizures
tial in selection of patients with refractory epilepsy
for surgical approaches [76].
Szlrgical Treatment
Numerous reports indicate that excision of epileptogenic foci can result in complete or nearly complete seizure relief in 60 to 80% of patients with
focal epilepsy refractory to anticonvulsant medications [ 5 , 7 , 14, 17, 35, 36, 4 1 , 4 2 , 58, 6 0 , 7 0 , 731.
Most often, the 20 t o 40% failure rate is attributed t o
inadequate resection or insufficient localization [6 1,
208 Annals of Neurology
Vol 9 No 3 March 1981
53% (in 56
64 76
64 %
62 5%
661. T h e major representative studies listed in Table
1 indicate several factors that support these postulated reasons for surgical failures. (1) Success is better with m o r e specific pathological lesions, e.g., 80%
in hamartomas [17, 22, 431. ( 2 ) Success is best with
temporal lobe foci, followed closely by occipital lobe
foci C601. ( 3 ) Results in children are comparable to
those in adults [17]. ( 4 )Surgical success declines with
limited resections [4, 731. An 80% success rate was
reported by Van Buren et al[73]in patients with total
temporal lobe excision (right, 6.2 cm; left, 4.8 cm) as
Intracerebral recording electrodes vary. A probe
designed by Charles Ray [631 is constructed by
laminating 18 wires around a length of 22-gauge needle and cutting the insulation to create one electrode
contact per wire at desired locations. This probe enables recording from numerpus sites simultaneously,
with precise montages selected for maximal demonstration of abnormalities. Some depth probes are
constructed with bundles of wires simply twisted together [63]. The wires may be wrapped around a
needle to provide some rigidity for introduction o r
may be introduced with a more rigid instrument,
which is then removed. Bipolar electrodes may be
used with contacts at their tips, with or without
a central core [57]. Electrodes are introduced
stereotactically with the patient under general
anesthesia; the usual targets selected include the
hippocampus, amygdala, medial frontal lobe, and
other possible areas as dictated by the particular seizure pattern and scalp EEG. Intraoperative or
preoperative air or radiopaque contrast visualization
of the ventricular system is used to define anatomical
structures. Crandall et a1 [ 151 have demonstrated the
stereotactic accuracy of one such method. Electrodes
are generally inserted through stainless steel guide
pins implanted firmly in the skull.
Some metals, especially silver, are toxic to the
brain and can produce abnormal EEG discharges.
Alloys in various combinations of platinum, iridium,
gold, stainless steel, nickel, and chromium as well as
several other metals are apparently nontoxic, as
demonstrated by histological study of cat brains after
implantation of intracerebral electrodes for more
than two months [12, 201.
Despite the feasibility of chronic depth recording of
the EEG in humans using stereotactically implanted
nontoxic depth probes, the use of depth EEG has
been shunned by several experts in the field of epilepsy surgery for various reasons [74]. A procedure
using blind introduction carries a small risk of intracerebral hemorrhage. Bacterial and aseptic meningitis are more common complications, but they can
be easily and successfully treated [13, 541. The
changes in cerebral microstructure accompanying
electrode implantation have not been studied in detail, but Brown [9] has examined some temporal lobe
specimens and noted only a strand of astrocytes along
the previous electrode site. Yet Rasmussen has
stated, “The ultimate risks of inserting electrodes
into the good hemisphere of a brain that has already
demonstrated its ability to generate a clinically
significant seizure tendency still await assessment”
Others have criticized the cost and the need for
210 Annals of Neurology
Vol 9 No 3
March 1981
special facilities. An estimate of $36,000 per patient
for complete evaluation, treatment, and follow-up is
likely to be accurate. The need for special personnel
and facilities is clear, but several such centers already
Difficulty with interpretation has also been a deterrent. Falconer, who did extensive epilepsy surgery in
England, never used depth recording. H e believed
that if the scalp EEG gave false localization, then
more “buried electrodes” would only provide additional uninterpretable information [7 11.
The most trenchant criticisms have been doubts
that such depth EEG recordings better localize an
epileptogenic area. Critics have objected that deep
recording cannot be accomplished from all possible
sites of abnormal activity, making the results no more
definitive than with scalp EEG. Well-documented reports exist of typical “temporal lobe seizure patterns”
with lesions of the occipital, parietal, and frontal
lobes 1671. These deficiencies might be acceptable if
it could be shown that depth EEG can increase surgical success despite known shortcomings. In other
words, it is still possible that the technique may be
better than scalp EEG, even though it is not perfect.
This major question has not been resolved.
The proponents of depth EEG have been prolific
in their documentation of benefits. The recording
method has been shown to contradict, confirm, or
add to the information obtained by routine scalp
EEG recording [ 2 , 29, 4 8 , 681. The lack of scalprecorded evidence of electrical activity observed in
the depths of the brain is frequently noted [ l ,8, 13,
16, 29, 45, 47, 48, 681. Depth EEGs are said to enable better localization of epileptogenic foci [ 16, 24,
27, 45, 4 6 , 4 8 , 49, 53, 571. Unsuspected multiple
foci can be detected [6, 7, 24, 48, 501. Conversely,
patients thought to have bilateral disease on the basis
of scalp EEG can be shown to have unilateral localized epileptogenic foci in the depths of the brain
[ 6 , 13, 24, 46-48, 50, 5 1 , 53, 5 5 , 57, 66, 721.
Many epileptologists believe that depth EEG is the
final word in the attempt to localize epileptogenic
foci [29, 51, 65, 7 5 , 761. If it is, it should improve
surgical success rates at those centers (including
UCLA, Paris, Montreal, and Yale) in which it is used.
But reported surgical success rates at these centers
remain 60 to SO%, no different from the rate in centers in which depth EEG is not used for surgical decisions [14, 5 5 , 60, 681.
The major difficulty in interpreting this information lies in the population of patients studied. Depth
EEG has generally been used only for patients with
equivocal scalp EEG localization. Chronic depth recording in the evaluation of candidates with refrac-
tory epilepsy is regularly employed only at UCLA
and Yale. Again, surgical results are no better than
when scalp recording is used [14, 681. But these
centers study many patients whose refractory epilepsy would not be considered surgically approachable at centers without the facilities for depth EEG,
because of t h e impossibility of otherwise localizing
an area for resection. Approached in this way, one
could conclude that depth EEG enables a surgical
success rate of 60 to 80% in a group of patients
otherwise considered unacceptable for surgery.
Furthermore, epilepsy surgery success statistics in
different eras should be compared. The potential
surgical population has changed over the past few decades. New anticonvulsant medications and the
ability to monitor serum anticonvulsant levels, now
used universally, have undoubtedly brought under
control a group of patients who formerly would
have been classified as medically refractory. The present population of patients whose epilepsy is considered medically refractory therefore has a more severe paroxysmal disorder in which the likelihood of
definition and surgical resection of a single paroxysmal focus might be expected to have a smaller chance
for success. The fact that surgical success rates have
not declined implies that methods have improved.
Depth EEG may also prevent needless surgery by
disproving scalp EEG localization. Though this potential use of the technique has not been extensively
discussed, I regard it as equally important.
Analysis of the Literatwe
I have systematically tabulated literature reports of
depth versus scalp EEG localizations. A critical approach was not possible because studies vary in terms
of recording techniques, electrode types and placement, and methods of information processing, storage, and presentation. For example, it is possible that
a much greater discrepancy will be found between
depth and scalp EEG data if scalp EEG records document only interictal activity from conventional
montages with the patient awake than if sleep
monitoring is done, or if ictal records are obtained
using montages that incorporate activity recorded
from nasopharyngeal o r sphenoidal leads. Published
reports often fail to clarify whether depth and scalp
EEGs were recorded simultaneously. The means of
patient selection for depth implantation vary from
center to center, further inhibiting comparisons.
Nevertheless, some answers are available.
Each report was reviewed, and scalp and depth
EEG localization were deduced from the data given
for ictal and interictal recording results. Ictal records
and their interpretations were not always available
for localization, but when they were cited, they were
given the most weight in a decision about localization
of the epileptogenic focus. Results of electrical
stimulation studies were included when available. In
several instances the same investigators published
several reports; whenever possible, duplication was
eliminated. When confusion arose or details were
given for only part of a group of patients, the remainder were noted as unspecified.
Using this information, patients were grouped into
one of five categories:
1. Scalp localization the same as depth localization
2. Scalp localization different from depth localization (both localized)
3. Scalp not localized or multifocal, depth well localized
4. Scalp localized, depth not localized or multifocal
5 . Scalp and depth both not localized or multifocal
For example, Bickford’s first patient [6] had right
temporal localization on interictal scalp as well as
depth recording. Electrical stimulation in the right
temporal area produced a seizure. Therefore, the patient was placed in category l (scalp localization the
same as depth localization), despite the lack of spontaneous seizures.
Table 2 gives details of the studies that included
sufficient data to compare scalp and depth EEG localization of epileptogenic foci. Table 3 summarizes
the results. Certain conclusions follow.
1. Depth EEG can select some patients with
medically refractory epilepsy for surgical therapy
who otherwise are not candidates because scalp EEGs
were not localized-i.e.,
all patients in category 3
with unlocalized scalp and localized depth EEG records. This amounts to an increase in operative candidates of 36% of patients reported (significance of
difference between proportions: Z = 5.40, p <
0.0 1).
2. Depth EEG can alter surgical plans or prevent
some needless surgery by demonstrating different,
multiple, or poorly defined foci, i.e., patients in categories 2 and 4. This amounts to a decrease in operative candidates amounting to 18% of patients reported ( Z = 3.60, p < 0.01). The experiences in
Milan [62] and Paris [69-711 are not categorized because data were not sufficiently detailed. However,
among patients studied by depth recording, 23% in
Milan and 35% in Paris were excluded from surgery,
presumably on the basis of the depth EEG; these too
are impressive numbers, though they may also include patients in category 5 .
3. Overall, in patients so far reported, depth EEG
could have altered surgical plans in more than
50%-i.e., all patients in categories 2, 3, and 4. The
experience at Johns Hopkins [47], excluded from
Neurological Progress: Spencer: Depth Electroencephalography 2 11
Table 2. Major Depth EEG Series with Localization by Category
No. of Patients by Category
Bickford [61, 1956
Crandall [13j, 1973
Crandall [14], 1975
Delgado and Hamlin [18], 1960
Delgado-Escueta e t a1 [131, 1779
Engel et a1 [211, 1979
Fischer-Williams and Cooper [24], 1963
Geier et a1 [ 2 8 ] , 1777
Kellaway [451, 1956
Kim [46], 1976
Laws et a1 1471, 1970
Lieb et a1 [48], 1976
Ludwig et a1 [49j, 1962
Ludwig et a1 [50], 1976
Maroserro et a1 [ 5 I], 1976
Niedermeyer et a1 [531, 1969
Olivier et a1 [55j, 1977
Rand et a1 [571, 1964
Ravagnati et a1 [ 6 2 ] , 1980
Rossi [651, 1773
Spencer et a1 1681, 1980
Talairach and Bancaud [691, 1973
Van Buren et a1 [731, 1975
t . .
Table 4. Surgical Results as Related t o Depth
versus Scalp E E G Localization
Table 3. Results of Review of Depth E E G Localization
i n 178 Presumptive Surgical Candidates
No. of
Percent of
categorization because of lack of detail, should be
noted here, with depth EEG findings of “significant
importance” in half the operated and all the nonoperated patients.
Although the tabulated studies are not strictly
comparable, the information justifies the need for
continued use and further evaluation of depth EEG.
Unfortunately, the data do not answer the question
of whether or not depth EEG localization of epileptogenic foci should be considered the final word.
Of the studies analyzed, only scattered mention is
made of surgical outcome in individual patients for
whom detailed EEG information is provided. Table 4
Annals of Neurology
Vol 7 N o 3 March 1981
Surgical Result No
Poor Surgery
Sample Good
breaks down outcome by the same categories used
before to compare scalp and depth EEG localization.
Even though the total number of patients in Table 4
(61 patients) is smaller than in Table 3 (178 patients),
the sample distribution across categories is comparable in the two tables. The success rate in otherwise
inoperable patients who had a focus resected that was
determined by depth EEG is seen to be 63% (category 3 patients)--comparable to the overall success
rate in most centers. In another way, this supports
the earlier conclusion that some patients with refractory epilepsy can be offered a chance for successful surgical treatment only by virtue of depth
EEG. Furthermore, in patients with localizing scalp
EEGs alone, predicted success is 67% (categories 1,
2 , and 4), yet surgical success is 85% among patients
in whom depth and scalp EEG localization agree (category 1).This comparison is worthy of consideration,
because it suggests that if all potential surgical candidates with localizing scalp EEGs were further evaluated by depth EEG, and patients were selected for
surgery only when localization by depth EEG
confirmed the scalp EEG focus, surgical success
would improve by nearly 20%. This difference is not
statistically significant because the numbers in Table
4 are small. More detailed reports are needed to substantiate these inferences.
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selection, depth, refractory, electroencephalography, surgery, epilepsy
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