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Extratemporal, nonlesional epilepsy in children: Postsurgical clinical and neurocognitive outcomes

Article (PDF Available) inJournal of Neurosurgery Pediatrics 7(2):179-88 · February 2011with41 Reads
DOI: 10.3171/2010.11.PEDS10265 · Source: PubMed
Abstract
Patients undergoing epilepsy surgery without evidence of a lesion on MR imaging and without a temporal source for seizure onset generally have less favorable outcomes than patients with structural lesions or temporal onset. However, many of these patients are viable candidates for invasive monitoring and subsequent resection or multiple subpial transections (MSTs). The purpose of this study was to evaluate the surgical treatment of pediatric patients with extratemporal, nonlesional epilepsy in order to better understand the clinical and neuropsychological outcomes expected in this patient group. Forty-three pediatric patients with negative results on MR imaging and lateralized, extratemporal findings on electroencephalography underwent invasive monitoring with grid and/or strip electrodes. Thirty-three subsequently had resection of an epileptogenic focus and/or MSTs. Outcome was classified as Engel class I or II in 54.5% of the patients who underwent resection/MSTs and Engel class III or IV in 45.5%. Use of MSTs was associated with poor outcome. Neuropsychological evaluation showed significant improvement in immediate auditory attention following surgery and revealed several significant results on subgroup analysis. Complications occurred in 14% of patients (a 7% rate per procedure). Ten patients (23%) underwent invasive monitoring without proceeding to therapeutic surgery because no epileptogenic region was amenable to resection. Neuropsychological outcomes were generally stable. Patients with extratemporal, nonlesional seizures are viable candidates for invasive monitoring with grid/strip electrodes, and good outcomes can be obtained with resective surgery. The use of MSTs may correlate with worse outcome. This study also provides additional data to assist in counseling patients on the risks of negative invasive monitoring, deficits resulting from resection/MSTs, and possible operative complications.
Figures
J Neurosurg: Pediatrics / Volume 7 / February 2011
J Neurosurg Pediatrics 7:000–000, 2011
179
The efcacy of surgical therapy in certain types of
epilepsy has been well established. A randomized
controlled trial has demonstrated that temporal
epilepsy patients, in particular, fare better with surgery,
achieving 58% seizure freedom in the rst year as com-
pared with 8% in the medically treated group.30 Further,
patients with demonstrable lesions on preoperative MR
imaging also showed favorable outcomes with surgery.
Several studies have demonstrated signicantly higher
rates of postoperative seizure freedom with “lesional”
epilepsy as opposed to “nonlesional” cases in tempo-
ral,5,12,14 extratemporal,33 and combined23 series. However,
the prognosis for seizure amelioration in patients without
temporal epileptogenesis or recognizable radiographic
lesions seems less certain. Two recent studies highlighted
the difculty in surgically treating extratemporal, nonle-
sional epilepsy. In one study7 involving 70 patients with
nonlesional epilepsy based on both MR imaging and
histopathology, the authors reported that Engel Class I
or II outcomes were achieved in only 33% of the extra-
temporal or temporal neocortical resection group com-
pared with 70% of the patients who underwent standard
temporal lobectomy. Similarly, in a study of 399 patients
undergoing epilepsy surgery,9 signicantly worse long-
J Neurosurg Pediatrics 7:179–188, 2011
Extratemporal, nonlesional epilepsy in children:
postsurgical clinical and neurocognitive outcomes
Clinical article
Ian G. DorwarD, M.D.,1,2 Jeffrey B. TITus, Ph.D.,1,3, 4 DavID D. LIMBrIck, M.D., Ph.D.,1,2
JaMes M. JohnsTon, M.D.,1,2 Mary e. BerTranD, M.D.,1,4 a nD MaTThew D. sMyTh, M.D.,1,2
1Pediatric Epilepsy Center and 3Department of Psychology, St. Louis Children’s Hospital; Departments of
2Neurosurgery and 4Neurology, Washington University School of Medicine, St. Louis, Missouri
Object. Patients undergoing epilepsy surgery without evidence of a lesion on MR imaging and without a tempo-
ral source for seizure onset generally have less favorable outcomes than patients with structural lesions or temporal
onset. However, many of these patients are viable candidates for invasive monitoring and subsequent resection or
multiple subpial transections (MSTs). The purpose of this study was to evaluate the surgical treatment of pediatric
patients with extratemporal, nonlesional epilepsy in order to better understand the clinical and neuropsychological
outcomes expected in this patient group.
Methods. Forty-three pediatric patients with negative results on MR imaging and lateralized, extratemporal
ndings on electroencephalography underwent invasive monitoring with grid and/or strip electrodes. Thirty-three
subsequently had resection of an epileptogenic focus and/or MSTs.
Results. Outcome was classied as Engel class I or II in 54.5% of the patients who underwent resection/MSTs
and Engel class III or IV in 45.5%. Use of MSTs was associated with poor outcome. Neuropsychological evaluation
showed signicant improvement in immediate auditory attention following surgery and revealed several signicant
results on subgroup analysis. Complications occurred in 14% of patients (a 7% rate per procedure). Ten patients
(23%) underwent invasive monitoring without proceeding to therapeutic surgery because no epileptogenic region
was amenable to resection. Neuropsychological outcomes were generally stable.
Conclusions. Patients with extratemporal, nonlesional seizures are viable candidates for invasive monitoring
with grid/strip electrodes, and good outcomes can be obtained with resective surgery. The use of MSTs may correlate
with worse outcome. This study also provides additional data to assist in counseling patients on the risks of negative
invasive monitoring, decits resulting from resection/MSTs, and possible operative complications.
(DOI: 10.3171/2010.11.PEDS10265)
key worDs      •      epilepsy surgery      •      invasive subdural electrode monitoring      •     
Engel class outcome      •      electrocorticography
179
Abbreviations used in this paper: AED = antiepileptic drug;
ECoG = electrocorticography; EEG = electroencephalogram; MST
= multiple subpial transection.
I. G. Dorward et al.
180 J Neurosurg: Pediatrics / Volume 7 / February 2011
term outcomes were noted in patients with extratemporal
(42% vs 74% Class I) or pathologically normal (62% vs
79% Class I) resections. Another study17 of pediatric pa-
tients showed 85% Engel Class I outcomes for temporal
versus 60% for extratemporal resections, though all cases
involved a pathological lesion.
We sought to evaluate outcomes of pediatric epilepsy
surgery in patients whose EEGs showed lateralizing nd-
ings but no temporal source, and whose MR images dem-
onstrated no potentially epileptogenic lesions. Though
studies have suggested that resective surgery for patients
with normal MR imaging studies,15 even when the source
is extratemporal,10,29 can yield satisfactory results, these
patients continue to pose a signicant challenge to the
epilepsy surgery team. We hypothesize that pediatric pa-
tients with extratemporal, nonlesional epilepsy will ben-
et from resective surgery in appropriate cases.
Methods
Following institutional review board approval, we
retrospectively reviewed the records of 141 consecutive
patients who presented to St. Louis Children’s Hospital
for invasive monitoring with subdural grid/strip electrode
placement between October 1994 and September 2007.
Of these, we identied 43 patients who did not undergo
temporal surgery (whether resection or MST), and whose
MR imaging scans demonstrated no abnormality that
corresponded with a likely seizure focus. All patients
were monitored with invasive video ECoG for a period of
3–21 days. Of these initial 43 patients in our study group,
33 underwent resection of an epileptogenic focus or, if the
area in question involved eloquent cortex, multiple sub-
pial transections (MSTs). One of these patients initially
underwent a round of negative intracranial monitoring,
but after a second attempt was able to proceed for an at-
tempted resection of an epileptogenic focus. Thus, for 10
children (23%), intracranial monitoring did not reveal a
resectable seizure focus or a localizable seizure onset, or
the family did not want to risk neurological decit associ-
ated with eloquent cortical resection, and these children
did not proceed to a therapeutic epilepsy surgery.
Preoperative Evaluation
We selected patients for invasive monitoring on the
basis of a comprehensive, multidisciplinary evaluation,
which included a complete history and physical exami-
nation, preoperative MR imaging, and video-monitored
scalp EEG. The MR imaging consisted of 1.5-T or 3.0-
T studies with a standard high-resolution epilepsy pro-
tocol. Other components of the preoperative evaluation
included functional MR imaging, interictal PET, ictal
SPECT, magnetoencephalography, and Wada testing in
some cases. A comprehensive neuropsychological assess-
ment established a developmental baseline and assisted
with localizing the seizure focus.
Surgical Procedure and Postoperative Evaluation
The rst procedure involved the implantation of cor-
tical electrode grids or strips with or without depth elec-
trodes. We typically performed intraoperative ECoG with
cortical stimulation motor mapping. The patients then
spent one night in the ICU followed by several days in
an epilepsy-monitoring unit with continuous video ECoG
monitor ing.
In 10 patients in whom we could not identify an epi-
leptogenic focus amenable to further surgery, the second
craniotomy involved only the removal of any implanted
grids/strips. For the remaining 33 patients in our study
group, the second craniotomy involved either a topecto-
my of ECoG-localized epileptogenic regions or MSTs (or
a combination of the two). All resected specimens were
submitted for full histopathological evaluation.
Postoperative radiological evaluation included plain
lms to conrm proper grid/strip placement on the day
of initial grid/strip implantation. The 33 study group pa-
tients further underwent MR imaging scanning after the
second stage of their procedures.
Nonlesional epilepsy patients were those in whom
no MR imaging evidence of an epileptogenic abnormal-
ity could be found. Despite having negative ndings on
preoperative MR imaging, some patients ultimately were
found to have epileptogenic substrates, such as cortical
dysplasia or microdysgenesis, on histopathological analy-
sis of their resected specimens; we did not exclude these
patients from the study, as this histopathologically based
diagnosis could not be made preoperatively and would
not be useful in the selection of surgical candidates.
Data Collection
Final long-term outcomes were graded utilizing the
Engel classication scheme.13 For statistical evaluation,
patients were grouped into Engel classes I and II (“good”
outcomes) or Engel classes III and IV (unsatisfactory out-
comes). Some studies have shown that seizure freedom
serves as the most important outcome measure in predict-
ing quality of life after epilepsy surgery;18,31 however, re-
cent work addressing extratemporal epilepsy surgery has
demonstrated that signicant psychosocial improvements
occur even without a seizure-free result.25,2 6
Positron Emission Tomography and SPECT
In patients for whom PET and SPECT results were
available (40/43 and 19/43 patients, respectively), these
ndings were categorized as being localizing or nonlocal-
izing, concordant or discordant with the location of inva-
sive grids/strips, and concordant or discordant with the re-
gion of resection or MSTs.
Magnetoencephalography and Wada Testing
Because magnetoencephalography and Wada testing
were employed rarely (1 and 2 cases, respectively), these
data were insufcient for analysis.
Electrocorticography
For patients whose ECoG data were complete and
accessible, ictal and interictal activity was categorized
as focal, multifocal, or poorly localized. We also noted
1) concordance between ictal and interictal activity and
2) completeness of resection of regions of ictal/interictal
activit y.
J Neurosurg: Pediatrics / Volume 7 / February 2011
Extratemporal nonlesional epilepsy outcomes
181
Pathological Analysis
All resected tissue was submitted for pathological
analysis. For statistical evaluation, we grouped these nd-
ings into normal pathology, focal lesion, or nonspecic
inammation/gliosis.
Neuropsychological Evaluation
All patients underwent a preoperative neuropsycho-
logical assessment that included standardized measures
of intellectual ability, academic achievement, ne mo-
tor skills, visual-spatial processing, language processing,
memory functioning, and executive functioning. Rating
scales completed by parents and teachers (when applica-
ble) helped characterize emotional and behavioral func-
tioning. A follow-up neuropsychological assessment after
surgery quantied changes in functioning and assisted
with treatment planning. When possible, measures from
the preoperative assessment were repeated at the time of
the follow-up assessment. Preoperative data and postop-
erative outcome data were compared when possible.
Statistical Analysis
Patient data are presented as means with SDs or
as a percentage of the number in a given group subset.
Probability values for group comparisons were obtained
using the chi-square test or Fisher exact test for categorical
variables and by unpaired t-test for continuous variables.
For analysis of neuropsychological outcomes, 32 neuro-
cognitive and neurobehavioral variables were evaluated
for pre- and postoperative differences using paired t-tests.
Subgroup analyses were also performed to assess for both
intragroup differences and pre- versus postoperative dif-
ferences for the following subgroups within each of the
32 variables: low and high IQ/performance, Engel class
I/II and III/IV, right- and left-sided surgery, frontal and
nonfrontal surgery location, and male and female sex.
Results
Patient Characteristics
Our 33-patient study group was composed of 18
males (54.5%) and 15 females (45.4%). Their mean age
was 3.85 years (range 0.17–11 years) at seizure onset and
11.63 years (range 3–19 years) at surgery. The mean dura-
tion of epilepsy was 7.64 years (range 0.5–16.25 years).
Of note, several of our poor-outcome patients underwent
further palliative procedures, including vagal nerve stim-
ulator placement (3 patients), corpus callosotomy (1 pa-
tient), and reattempted invasive monitoring and topecto-
my (1 patient); their outcomes were not affected by these
further interventions.
Table 1 presents demographic characteristics, preoper-
ative seizure characteristics, complications, and procedural
data according to Engel class outcome. No signicant dif-
ferences in demographic variables were noted between the
Engel class I/II and III/IV groups.
Preoperative Evaluation
Whether PET and SPECT ndings were localizing,
concordant with grid/strip location, or concordant with
the ultimate site of resection or MSTs did not show any
statistically signicant associations with the likelihood of
proceeding to therapeutic resection/MSTs or with Engel
class outcomes (Tables 2 and 3).
Table 4 presents a comparison of ECoG data accord-
ing to Engel class outcome. The only signicant difference
noted between the Engel class I/II and III/IV groups was
that the former more frequently experienced a complete re-
section of their region of ictal onset. A nonsignicant trend
for better outcome was also observed for patients with a
complete resection of the zone of interictal epileptiform
activity (p = 0.1).
Outcomes: Engel Class
Fourteen (42.4%) of the 33 patients undergoing ther-
apeutic epilepsy surgery with either resection or MSTs
achieved an Engel class I outcome, while 18 (54.5%) had
either Engel class I or II outcome. Table 5 presents the
Engel classication outcomes of all patients and those
with more than 2 years’ follow-up.
The length of follow-up between groups was also sub-
jected to statistical evaluation, and while no signicant dif-
ference was realized, we did note a nonsignicant trend
toward shorter follow-up duration between Engel class I/II
patients and Engel class III/IV patients (37.6 ± 23 vs 63.6
± 46, p = 0.06).
Surgery Type and Location
Please refer to Table 1 for presentation of procedure
type and location according to Engel class outcome. Having
undergone resection plus MSTs was signicantly associated
with Engel III/IV outcome (p = 0.004); a signicant asso-
ciation was also noted (p = 0.05) between having under-
gone any MSTs and being in the Engel class III/ IV outcome
group.
Pathologic Evaluation
Results of pathological evaluation are also shown in
Table 1. The focal lesions that were identied in our patients
included cortical dysplasias, microdysgenesis, and subcor-
tical white matter heterotopias. No signicant differences in
Engel class outcome were noted between the normal cortex,
focal lesion, and inammation/gliosis groups.
Complications and Postoperative Decits
Three of the 43 original patients undergoing cranioto-
my for invasive monitoring experienced wound infections:
one developed a stitch abscess, one suffered a fall that
caused acute wound dehiscence and ultimately osteomy-
elitis of his bone ap, and another experienced dehiscence
of his wound. All of them required simple irrigation and
debridement or repeat craniotomy for wound irrigation/de-
bridement. Other unexpected returns to the operating room
occurred because of symptomatic pneumocephalus in 1
patient, and removal or fracture of electrodes secondary to
patient manipulation in 2 others. Other complications in-
cluded a case of aseptic meningitis, a frontalis nerve palsy,
and a blood transfusion. Overall, complications requiring
an unanticipated surgical procedure developed in 6 cases
I. G. Dorward et al.
182 J Neurosurg: Pediatrics / Volume 7 / February 2011
TABLE 1: Demographic and characteristics by Engel class (I/II vs III/IV)*
Variable
Postop Engel Class
p ValueI & II (18 patients) III & IV (15 patients)
patient characteristics
sex 0.90
female 8 (44) 7 (47)
male 10 (56) 8 (53)
mean age (yrs) at seizure onset 4.24 ± 2.8 3.82 ± 2.8 0.67
mean age (yrs) at op 12.2 ± 4.8 11.1 ± 4.7 0.52
no. of AEDs tried 5.39 ± 1.8 5.67 ± 1.8 0.67
history of status epilepticus 1 (6) 3 (20) 0.31†
history of trauma 1 (6) 2 (13) 0.58†
family history of seizures 5 (28) 3 (20) 0.70†
length of FU 37.6 ± 23 63.6 ± 46 0.06
pathology 0.77†
normal 8 (44) 6 (43)
focal lesion 9 (50) 6 (43)
    inammation or gliosis alone 1 (6) 2 (14)
study half period 0.65
1 7 (39) 7 (47)
2 11 ( 61) 8 (53)
surgeon 0.75†
J.G.O. 6 (33) 3 (20)
M.D.S. 8 (44) 7 (47)
T. S . P. 4 (22) 5 (33)
seizure characteristics
type 0.54†
simple partial 1 (6) 2 (13)
complex partial 10 (56) 7 (47)
generalized 5 (28) 2 (13)
multiple types 2 (11) 4 (27)
duration 7.94 ± 4.5 7.28 ± 4.6 0.68
yearly seizure burden 0.15†
mean no. of seizures 1829 ± 2275 1254 ± 2173
median no. of seizures 912 182
complications & neurological decits
    any complication or neurological decit 10 (56) ‡ 10 (67) 0.52
    decit type† 0.1
none 8 (44) 5 (33)
temporary 6 (33) 3 (20)
permanent 4 (22) 7 (47)
    permanent decit 4 (22) 7 (47) 0.1 4
procedure
any MSTs 0.05†¶
no 16 (89) 8 (53)
yes 2 (11) 7 (47)
(continued)
J Neurosurg: Pediatrics / Volume 7 / February 2011
Extratemporal nonlesional epilepsy outcomes
183
(in 14% of the original 43 patients, or after 7% of the 86
procedures with electrode placement and therapeutic sur-
gery and/or removal). In 3 of these cases (7% of patients,
3.5% of procedures) wound infections necessitated a return
to the operating room.
Some proportion of our patients also experienced ei-
ther temporary or permanent neurological decits after
surgery (refer to Table 6 for details of neurological de-
cits), which we consider distinct from surgical complica-
tions for reasons to be elaborated in the Discussion. For
comparison between Engel classes I and II and classes III
and IV with respect to neurological decits, please refer
again to Table 1. No signicant differences were noted
between groups.
Neuropsychological Outcome
Twenty-three patients underwent both pre- and postop-
erative comprehensive neuropsychological assessments. The
mean interval between the pre- and postoperative assess-
ments was 17.65 months (range 8–75 months). Comparison
of the per formance of the entire sample pre- and post surgery
revealed generally stable intellectual functioning. Overall
intelligence remained stable regardless of gender, seizure
out come, or level of pre op er at ive ful l-scale IQ. Childr en who
had surgery to their left cerebral hemisphere demonstrated
signicant postsurgical improvements in performance IQ (p
= 0.002) that may have been due to primary improvements
in their performance on a measure of nonverbal reasoning
(p = 0.06). Children who had surgery to their right cerebral
hemisphere displayed stable performance IQ scores postsur-
gically. For verbal IQ, no signicant changes were observed
following either left-sided or right-sided surgery, and no
changes in intellectual performance were noted based upon
TABLE 1: Demographic and characteristics by Engel class (I/II vs III/IV)* (continued)
Variable
Postop Engel Class
p ValueI & II (18 patients) III & IV (15 patients)
procedure (continued)
resection & MSTs 0.004†
no 18 (100) 9 (60)
yes 06 (40)
frontal resection 0.74
no 7 (39) 5 (33)
yes 11 ( 61) 10 (67)
parietal resection 1.0†
no 16 (89) 13 (87)
yes 2 (11) 2 (13)
occipital resection 1.0†
no 15 (83) 13 (87)
yes 3 (17) 2 (13)
* Data are numbers of patients (% of group) unless otherwise indicated. Means are given with SDs. Probability values are for
comparison of groups by chi-square test (for categorical variables) or unpaired t-test (for continuous variables), unless otherwise
indicated. Patients with both permanent and temporary complications are classied in the permanent categor y. Abbreviation: FU 
= follow-up.
† By Fisher exact test or Wilcoxon test (for yearly seizure burden).
‡ Percentages based on the 33 patients undergoing resection/MSTs, not the total of 43 who underwent invasive monitoring.
§ By Cochran-Armitage trend test.
¶  Statistically signicant.
TABLE 2: Association of PET and SPECT variables with having
undergone a therapeutic procedure*
Variable
Therapeutic Procedure p
Value†No Yes
PET localizing 0.27
no 6/10 (60) 11/30 (37)
yes 4/10 (40) 19/30 (63)
PET concordant w/ grid/strip
location
0.15
no 7/10 (70) 12/30 (40)
yes 3/10 (30) 18/30 (60)
SPECT localizing 0.63
no 2/6 (33) 7/13 (54)
yes 4/6 (67) 6/13 (46)
SPECT concordant w/ grid/strip
location
1.0
no 4/6 (67) 8/13 (62)
yes 2/6 (33) 5/13 (38)
* Values represent numbers of patients (%). Ten patients underwent
monitoring (twice in 1 case) without proceeding to therapeutic surgery;
33 patients underwent therapeutic surgery after monitoring.
† By Fisher exact test.
I. G. Dorward et al.
184 J Neurosurg: Pediatrics / Volume 7 / February 2011
the location of the surgery (that is, frontal or nonfrontal).
Nevertheless, there was a trend toward improved perfor-
mance on an intellectual measure of verbal abstract reason-
ing among all children who achieved better seizure control
(p = 0.07).
Further analyses of neuropsychological outcomes
revealed unchanged performance in most domains. On
a measure of verbal learning using the California Verbal
Learning Test, learning efciency and long-term recall
remained unchanged, regardless of sex, surgery location,
prior level of functioning, or seizure outcome. The same
was true on measures of visual memory. However, children
with poorer seizure outcome after surgery (Engel Class III
or IV) displayed a signicant decline in their abilities to
recall structured verbal information (stories) (p = 0.04). In
terms of executive functioning, signicant improvements
in immediate auditory attention were observed for the en-
tire sample (p = 0.05), and further analyses suggested a
trend toward improved attention among children who had
surgery to their right cerebral hemisphere (p = 0.08).
Discussion
Multiple studies have documented the efcacy of re-
sective epilepsy surgery, with 2 principal determinants of
success: whether a discrete resectable lesion exists, and
whether the targeted epileptogenic region is in a temporal
or extratemporal location. Evidence has begun to accumu-
late regarding the treatment of patients with extratemporal,
nonlesional epilepsy. Surgery for these patients has gen-
erally yielded Engel class I or II outcomes in 33%–61%
of patients. However, one study—similar in design to our
study, but in patients aged 8–28 years—showed excellent
outcomes, with 81% of patients rendered seizure-free and
all patients having a > 90% reduction in seizures;10 their
sample size was relatively small (16 patients), and this de-
gree of success has not been duplicated in other studies.
Aside from this study, our 54.5% rate of Engel class I and
II outcomes compares favorably with other ndings in the
literature, including a recent meta-analysis of extratempo-
ral, nonlesiona l epilepsy surgery in which an overall 48.4%
rate of Engel I or II outcomes was obtained for 95 patients
in 17 retrospective studies.1 Of course the surgeon’s selec-
tion of operative candidates may substantially impact out-
come in these cases, and as such has the potential to intro-
duce selection bias in this and any related study. Unlike
these previous studies, however, we have included only
pediatric patients, thereby improving the generalizability
of our results for the pediatric population.
The principal utility of this study is to support further
the idea that good or excellent outcomes can be obtained
in extratemporal, nonlesional epilepsy cases despite what
is often thought to be a poor surgical prognosis. Our
ndings may also prove useful to epilepsy surgeons in
counseling families regarding the likelihood of seizure
freedom or amelioration following surgery. An impor-
tant point of emphasis is the potential for subjecting the
patient to invasive monitoring with subdural grids and
strips, yet nding no region of epileptogenic cortex ame-
nable to topectomy or MSTs. In our study, 43 patients un-
derwent invasive monitoring, with only 33 proceeding to
therapeutic epilepsy surgery; thus our patients had a 23%
risk of undergoing an invasive study with negative results.
This compares with our earlier series of 112 consecutive
patients undergoing invasive monitoring in the study by
Johnston et al.16 in which 17 (15.2%) of 112 patients did
not proceed to a therapeutic procedure. If we include the
next 29 consecutive invasively monitored patients since
the cut-off date of the aforementioned study, this rate
drops to 17 of 141, or 12.1%. This risk of negative results
from invasive monitoring is consistent with the challeng-
ing surgical management of extratemporal, nonlesional
epilepsy, and must be emphasized to patients and families
to create realistic expectations.
We did not identify any preoperative prognostic fac-
tors to identify patients who would most likely benet
from invasive monitoring or from a therapeutic resec-
tion or MST. The results of PET and SPECT, though not
available in all cases, showed no association with either
the likelihood of proceeding to a therapeutic surgery
following invasive monitoring or with Engel Class out-
come. This negative nding suggests that in the subset
of patients with extratemporal, nonlesional epilepsy, these
preoperative diagnostic adjuncts may not contribute sub-
stantially to surgical decision making. However, such a
TABLE 3: Association of PET and SPECT variables with Engel
Class in patients who have undergone a therapeutic procedure
Variable
Engel Class
p
Value*
I or II
(18 patients)
III or IV
(15 patients)
PET localizing 0.7
no 6/15 (40) 5/15 (33)
yes 9/15 (60) 10/15 (67)
PET concordant w/ resection/
MS Ts
0.44
no 11/15 (73) 9/15 (60)
yes 4/15 (27) 6/15 (40)
PET concordant w/ grid/strip
location
0.46
no 7/15 (47) 5/15 (33)
yes 8/15 (53) 10/15 (67)
SPECT localizing 1. 0†
no 4/7 (57) 3/6 (50)
yes 3/7 (43) 3/6 (50)
SPECT concordant w/ resection/
MS Ts
0.56†
no 6/7 (86) 4/6 (67)
yes 1/7 (14) 2/6 (33)
SPECT concordant w/ grid/strip
location
0.59†
no 5/ 7 (71) 3/6 (50)
yes 2/7 (29) 3/6 (50)
* Unless otherwise indicated, p values refer to comparison of groups
by chi-square test.
† By Fisher exact test.
J Neurosurg: Pediatrics / Volume 7 / February 2011
Extratemporal nonlesional epilepsy outcomes
185
conclusion would need to be validated in a larger series
of patients. Further, regarding invasive ECoG data, we
noted that only the completeness of resection of a region
of ictal onset correlated with improved outcome; this re-
sult corroborates earlier ndings.7 A nonsignicant trend
was also noted between completeness of resection of the
interictal zone of activity and improved Engel class out-
come, and we might anticipate a more robust result with a
larger sample size. We did not nd any particular electri-
cal characteristics on preoperative EEG or intraoperative
ECoG that correlated with outcomes. In contrast, a re-
cent study showed that focal high-frequency oscillations
at seizure onset correlated with increased likelihood of
Engel class I outcomes.29
An important design element in this study is that
we selected “nonlesional” patients on the basis of preop-
erative MR imaging alone. This approach contrasts with
some other studies in which the determination of lesional
versus nonlesional status was made on the basis of patho-
logical ndings. We consider the former approach more
clinically useful, as MR imaging is readily available in
the period of preoperative assessment and is vital in de-
termining optimal candidates for epilepsy surgery and
in counseling patients and families. Of course, utilizing
imaging rather than pathology to make the determination
of “lesional” versus “nonlesional” might lead to the inclu-
sion in our study of some patients who would have been
excluded from previous studies.7 On the other hand, com-
pleteness of resection is an important determinant of out-
come with epileptogenic lesions; the fact that we lacked
imaging to guide the completeness of resection could be
seen as a cause of worse outcomes. In sum, our method of
dening “nonlesional” cases might introduce bias, but the
direction of this bias remains unclear.
One important limitation of our study relates to the
duration of follow-up, which varied somewhat (though
nonsignicantly, p = 0.06) between our outcome groups,
with Engel class I and II patients having shorter duration
of postoperative follow-up. This factor could bias our re-
sults, as some of these seizure-free or “good outcome” pa-
tients might have manifested worse clinical outcomes had
our follow-up duration been longer. On the other hand, if
a patient’s epilepsy has been “cu red” or signicantly ame-
liorated, the patient’s parents might be less likely to make
the effort to maintain contact with the epilepsy manage-
ment team. Thus, while this shorter follow-up duration
in patients with good or excellent outcome represents a
source of possible bias, it may be the direct result of those
better outcomes.
A certain number of our ndings were notable in that
TABLE 5: Outcomes of surgery (Engel classication)
Engel Class All Patients (33 patients)
Patients w/ >2 yrs FU
(22 patients)
I14 (42) 8 (36)
II 4 (12) 3 (14)
III 10 (30) 7 (32)
IV 5 (15) 4 (18)
TABLE 4: Comparison of ECOG data by Engel class in 26 patients*
Variable
Engel Class
p ValueI or II (14 patients) III or IV (12 patients)
ictal onset focal, multifocal, or poorly localized 1.0†
focal 9 (64) 7 (58)
multifocal 2 (14) 2 (17)
poorly localized 2 (21) 3 (25)
interictal onset focal, multifocal, or poorly localized 0.88
focal 5 (36) 4 (33)
multifocal 7 (50) 5 (42)
poorly localized 2 (14) 3 (25)
ictal activity matches interictal activity 0.67
no 7 (50) 7 (58)
yes 7 (50) 5 (42)
ictal onset completely resected 0.05‡
no 2 (14) 6 (50)
yes 12 (86) 6 (50)
interictal activity region completely resected 0.1
no 6 (43) 9 (75)
yes 8 (57) 3 (25)
* Data are the number of patients (percentage of group). Unless otherwise indicated, p values are for comparison of groups by
chi-square test.
† Due to sparse data in the cross-tabulations, p values by Fisher exact test.
‡  Signicant at the p = 0.05 level.
I. G. Dorward et al.
186 J Neurosurg: Pediatrics / Volume 7 / February 2011
they did not show signicant association with seizure out-
come. For instance, we did not note that outcomes cor-
related with preoperative seizure frequency or duration,
though these relationships have been established in ex-
tratemporal epilepsy surgery;8,9 this nding likely stems
from the relatively small sample of patients meeting in-
clusion criteria for our study (compared with 81 and 399
patients, respectively, in the referenced studies), as well
as the heterogeneity of our study population. Further, the
presence of a pathological abnormality in the resected
specimen—such as focal cortical dysplasia, microdysgen-
esis, or heterotopia—did not correlate with seizure out-
come. While our study may have been underpowered to
detect a difference between groups, these results suggest
that from the standpoint of “lesional” epilepsy, the fact
of a lesion being radiographically evident on MR imag-
ing may be more clinically signicant than its presence
upon pathological study. Pertinent to this issue, it must
be noted that none of our patients’ pathological samples
showed neoplasia, the presence of which has been shown
to be useful in predicting outcomes for extratemporal epi-
lepsy surgery.8 A recent study
33 found a signicant cor-
relation between nonneoplastic focal lesions and surgical
outcome, but 94% of these lesions were apparent on pre-
operative MR images.
Multiple Subpial Transections
One of the other signicant ndings in this study
was that patients who underwent MSTs were more likely
to have a poor seizure outcome. These data should not
necessarily impugn the efcacy of MSTs—which has
been addressed elsewhere4,6,11,19–22, 24,32—as the study was
neither designed nor adequately powered to address that
issue. However, the fact of MSTs having been performed
may be a negative predictor of outcome because their
use indicates that a region of ictal onset or early spread
remains in situ. At our institution, previous work2 has
demonstrated that in patients with rolandic epilepsy, to-
pectomy is superior to MST for seizure outcome, but
that MSTs can be performed safely in eloquent cortex,
without resultant decits. Thus, at our institution MSTs
are performed in patients with ictal onset or early spread
involving eloquent cortex, the resection of which would
likely result in a neurological decit. If, after extensive
family discussion, the preference is to err on the side
of avoiding neurological decit even if it means leaving
potentially epileptogenic tissue in place, then we tend to
offer MSTs as a safer alternative, albeit one that is in-
ferior from the standpoint of seizure control. Our nd-
ings in this study do not generally add to the knowledge
regarding MSTs, except to say that in this group of pa-
tients with extratemporal, nonlesional epilepsy they were
largely ineffective—hence the association with Grade III/
IV outcomes—except for one successful case (one patient
with a Grade I outcome had exclusively MSTs). Further,
as in our institution’s previous study of rolandic epilepsy,2
MSTs were generally safe, with no neurological decits
directly attributable to their use.
Neuropsychological Outcomes
Our results suggest generally favorable neurocogni-
tive outcomes in children who undergo nonlesional, ex-
tratemporal lobe epilepsy surgery, with stable intellectual
functioning in the sample as a whole and evidence of
improvements in specic aspects of intelligence (that is,
performance IQ) among children who undergo surgery to
TABLE 6: Neurological decits associated with topectomy*
Case
No.
Age
(yr s) Op Neurological Decit
FU
(mos) Status at Final FU
Engel
Class
114 occipital cortex resection lt homonymous hemianopsia 27 subtle persistent visual eld defect  I
2 5 frontal cortex resection supplementary motor area syndrome 25 no residual decit I
311 frontal cortex resection lt hemiparesis 74 left spastic hemiparesis, 3–4/5 strength I
4 7 occipital cortex resection lt lat visual eld decit 14 persistent decit I
516 frontal cortex resection Broca aphasia 79 no residual decit I
612 frontal cortex resection supplementary motor area syndrome 37 no residual decit I
718 frontal cortex resection supplementary motor area syndrome 20 no residual decit III
817 frontal cortex resection lt hemiparesis 37 4+/5 lt UE paresis III
916 frontal cortex resection lt hemiparesis 67 no residual decit I
10 8frontal cortex resection supplementary motor area syndrome 120 no residual decit III
11 3occipital cortex resection visual eld decit 25 no residual decit I
12 17 frontal/parietal cortex resection expressive aphasia 39 persistent but improved speech uency
  decit
III
13 19 frontal cortex resection rt hemiparesis 42 persistent but improved right hemiparesis I
14 10 frontal cortex resection exacerbation of preexisting rt UE paresis 20 improved but persistent rt UE paresis III
15 7frontal cortex resection lt hemiparesis 164 persistent but improved left hemiparesis IV
16 17 frontal cortex resection supplementary motor area syndrome 42 slight hyperreexivity but no motor decit I
17 12 frontal/parietal cortex resection lt facial paresis 17 mild persistent facial paresis IV
* UE = upper extremity.
J Neurosurg: Pediatrics / Volume 7 / February 2011
Extratemporal nonlesional epilepsy outcomes
187
their left cerebral hemisphere. It is possible that children
who underwent left-sided surgery may have experienced
signicant improvements in nonverbal reasoning (that is,
matrix reasoning) secondary to reduced seizure activ-
ity in their right cerebral hemisphere; improved seizure
control may have allowed their unaffected cerebral hemi-
sphere to function more efciently. Unfortunately, the va-
lidity of this conclusion cannot be denitively evaluated
due to limited information about functional organization
in the present sample (that is, hemispheric dominance).
Patients displayed generally stable neurocognitive
performance in other areas as well. No signicant chang-
es were observed in visual-spatial processing or language
processing, and most aspects of memory functioning re-
mained well-preserved following surgery. Children with
Engel Class III or IV outcomes did demonstrate a sig-
nicant decline in their ability to recall meaningful ver-
bal information (stories), though this decline was not ob-
served in other subsamples in the current study. It is pos-
sible that children with poor seizure outcome, left-sided
surgery, and/or low presurgical intelligence may be at risk
for poorer verbal memory outcomes, though further in-
vestigation would be necessary to explore this conclusion.
It should also be noted that this decline in verbal memory
may reect cognitive side effects from the AED regimen
of children with poor seizure outcomes, as AEDs are
known to impact memory and executive function.28
Declines in executive functioning are one of the most
prominent concerns when considering extratemporal sur-
gery, particularly when the frontal lobes are involved. Our
results do not show declines in executive functioning, but
instead highlight improvements in selected aspects there-
of. For example, the previously discussed improvement in
nonverbal reasoning among children who underwent left-
sided surgery may suggest benets in aspects of executive
functioning that are not anatomically associated with the
location of the surgery. Moreover, our results reveal signi-
cant improvements in immediate auditory attention (digit
span) for the entire sample, with a trend toward specic
improvements among children who underwent surgery
to their right cerebral hemisphere. While this nding is
encouraging, we should emphasize that the impact of re-
ductions in AEDs among children who experienced bet-
ter seizure outcomes cannot be ruled out as a contributing
factor. Importantly, the current study also does not provide
information about emotional and/or behavioral outcomes
among children who undergo surgery. Children with epi-
lepsy, especially intractable epilepsy,27 are at increased risk
for internalizing psychopathology (such as depression and
anxiety). Therefore, improvements in attention may occur
in accordance with the improvements in emotional func-
tioning associated with better seizure control.
In evaluating our neuropsychological results, it should
be noted that we performed a large number of statistical
tests in exploring the interactions between patient subsam-
ples and various neurocognitive evaluations; as such, the
likelihood of obtaining falsely positive statistical correla-
tions is increased.
Complications and Postoperative Decits
A salient feature of our results is the seemingly large
proportion of patients sustaining either a temporary
(28%) or permanent (32%) neurological decit. It is essen-
tial to understand that, in this series, all but one (a tran-
sient frontalis palsy) of these outcomes were predictable
on the basis of the procedure performed, and were fully
discussed with the patient and family prior to proceeding.
The nature of surgery in this group of epilepsy patients
is that resection of epileptogenic cortex necessarily im-
plies some loss of function; in ideal circumstances this
loss of function is clinically silent, but in some cases it
involves an expected postoperative decit. This inherent
trade-off of function for possible seizure amelioration is
something that must be discussed at length with patients
and families in the course of preoperative counseling and
decision making. In any event, in those cases in which
decits were expected, we did not look upon temporary
or permanent decits as complications per se, because of
their inherent predictability. On the other hand, our pa-
tients suffered 3 wound infections and 3 additional com-
plications, leading to a 14% risk per patient, or a 7% risk
per procedure, of unpredicted complications; when the
need for electrode repositioning is excluded, our rate falls
to 9.3% of patients or 4.7% of procedures. Overall, our
complication rate is somewhat higher than the 4%–5.4%
rate reported in some larger studies of epilepsy surgery,3,9
but it remains relatively close to the 7.4% rate of compli-
cations requiring reoperation (not including reoperation
for grid/strip adjustment) in our recently published expe-
rience with invasive monitoring in 112 procedures.16
Conclusions
Surgery for seizures of extratemporal, nonlesional
origin remains challenging. In this pediatric-only study,
we have demonstrated that these patients are viable can-
didates for invasive monitoring with grid/strip electrodes,
and good outcomes can be obtained with resective sur-
gery. Important points to highlight in preoperative dis-
cussions with patients and families include the risk of
invasive monitoring without a subsequent therapeutic
procedure and the possibility of incurring a minor neuro-
logical decit as a trade-off for a chance at seizure ame-
lioration.
Disclosure
The authors report no conflict of interest concerning the mate-
rials or methods used in this study or the findings specified in this
paper.
Author contributions to the study and manuscript preparation
include the following. Conception and design: Smyth, Dorward,
Titus. Acquisition of data: Dorward, Johnston, Titus. Analysis and
interpretation of data: Smyth, Dorward, Titus, Johnston, Bertrand.
Drafting the article: Dorward. Critically revising the article: Smyth,
Dorward. Reviewed final version of the manuscript and approved it
for submission: all authors. Administrative/technical/material sup-
port: Dorward. Study supervision: Smyth.
Acknowledgments
The authors acknowledge Karen Steger-May for assistance
with statistical evaluations and Karen Dodson for assistance with
manuscript preparation.
I. G. Dorward et al.
188 J Neurosurg: Pediatrics / Volume 7 / February 2011
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Manuscript submitted June 18, 2010.
Accepted November 8, 2010.
Portions of this study were presented at the American Society of
Pediatric Neurosurgeons 2008 Annual Meeting, February 3–8, at
Los Cabos, Mexico.
Address correspondence to: Matthew D. Smyth, M.D., Department
of Neurosurgery, St. Louis Children’s Hospital, Washington
University School of Medicine, One Children’s Place, Suite 4S20,
St. Louis, Missouri 63110-1002. email: smythm@nsurg.wustl.edu.
  • ... Approximately 26% of children with MRI-negative DRE were seizure-free in our series after a mean follow-up of 2.8 years. Other pediatric series have reported seizure-free outcomes in 36–48% of patients [2,[13][14][15]22]. In relatively ''traditional'' patients (single semiology and concordant ictal EEG), our seizure-free proportion (50.0%) was comparable to these reports, and higher than our ''non-traditional'' patients (15.2%). ...
  • ... As a consequence, Engel class I seizure freedom rates vary considerably. In general, most studies demonstrate ~50–70 % seizure freedom at 1–2 years [13][14][15][16][17][18][19][20][21][22][23][24][25] with a decrease in seizure freedom rates at 5-and 10- year follow-up to ~30–60 % [14, 17, 18,[26][27][28][29]. Given the long-term prognosis of medically intractable epilepsy patients, however, seizure freedom rates on this order likely still represent a significant improvement over continued medical therapy . ...
  • ... Factors that correlated with good outcome were the presence of convergent scalp EEG, focal interictal spikes (p<0.005), and completeness of resection (p<0.0005). Dorward et al. (2011) studied children with extratemporal, nonlesional epilepsy. Outcome was classified as Engel class 1 or 2 in 54.5% of the children who underwent resection of the lesion or multiple sub-pial resections. ...
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