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RESEARCH PAPER
Complications to invasive epilepsy surgery workup
with subdural and depth electrodes: a prospective
population-based observational study
Emelie Hedegärd,
1
Johan Bjellvi,
1
Anna Edelvik,
1
Bertil Rydenhag,
1
Roland Flink,
2
Kristina Malmgren
1
1
Epilepsy Research Group,
Institute of Neuroscience and
Physiology, Sahlgrenska
Academy at Gothenburg
University, Göteborg, Sweden
2
Department of Clinical
Neurophysiology, Uppsala
University Hospital, Uppsala,
Sweden
Correspondence to
Professor Kristina Malmgren,
Epilepsy Research Group,
Institute of Neuroscience and
Physiology, Section of Clinical
neuroscience and
Rehabilitation Per Dubbsgatan
14 1 tr, Sahlgrenska Academy
at Gothenburg University,
413 45 Göteborg Sweden;
Kristina.malmgren@neuro.gu.
se
Received 2 August 2013
Revised 11 November 2013
Accepted 13 November 2013
To cite: Hedegärd E,
Bjellvi J, Edelvik A, et al.
J Neurol Neurosurg
Psychiatry Published Online
First: [please include Day
Month Year] doi:10.1136/
jnnp-2013-306465
ABSTRACT
Objective In some patients who undergo presurgical
workup for drug-resistant epilepsy invasive seizure
monitoring is needed to define the seizure onset zone
and delineate eloquent cortex. Such procedures carry
risks for complications causing permanent morbidity and
even mortality. In this study, prospective data on
complications in a national population-based sample
were analysed.
Design Complication data from the prospective
Swedish National Epilepsy Surgery Register were
analysed for 271 patients in whom therapeutic surgery
was preceded by invasive monitoring 1996–2010.
Results Complications occurred in 13/271 patients
(4.8%). Subdural grids carried the highest risk of
complications (7.4%). There was no surgical mortality or
permanent morbidity. Subdural haematomas were most
common (n=7) followed by epidural haematomas (n=3).
Valproate treatment and having a haematoma was
associated with an OR of 1.53 (CI 0.38 to 6.12)
compared to having a haematoma without valproate
treatment. Having a complication during invasive
monitoring was associated with a significant OR of 6.27
(CI 1.32 to 29.9) of also having a complication at
therapeutic surgery compared to the risk of having a
complication only at surgery.
Conclusions In this prospective population-based
epilepsy surgery series, the most common complications
were haematomas, and subdural grids carried the
highest risk. Close supervision and rapid interventions
led to avoidance of permanent morbidity. The clinical
implications of the slightly increased risk of haematomas
with valproate treatment needs further investigation as
does the finding of an increased risk for complications at
epilepsy surgery for patients who had a complication
during invasive monitoring.
INTRODUCTION
Epilepsy surgery is an established treatment in
selected patients with drug-resistant epilepsy result-
ing in seizure freedom or a significant reduction of
seizure frequency in the majority of operated
patients.
1–3
A detailed clinical assessment is critical before a
decision about surgery can be made in order to
localise the seizure onset zone. For many patients, a
non-invasive presurgical workup is satisfactory.
However, especially in MRI-negative patients, inva-
sive seizure monitoring is required for localising
the seizure onset zone and also for delineating the
area of planned resection against eloquent cortex.
4
Despite the potential benefits of the invasive
workup, they have to outweigh the risks related to
the neurosurgical procedure. The rates of reported
complications related to invasive monitoring differ
widely between studies, from no complications at
all
5
up to 26.3%.
6
The reasons for these varying
proportions may be related to the definitions of
complications and to study methodology (eg, if
data are obtained retrospectively or prospectively).
Different classifications of complications have
been suggested. Many reports use the terms transi-
ent and permanent,surgical and neurological com-
plications.
78
Additionally, severity scales from 1 to
4,
9
or from 1 to 5 have been used.
4
In the Swedish
National Epilepsy Surgery Register all complica-
tions related to diagnostic or therapeutic epilepsy
surgery procedures are reported and are graded as
major or minor.
10
A few studies have evaluated the usefulness and
safety versus the risks associated with implantation
of intracranial electrodes, and the benefits of inva-
sive workup for epilepsy surgery in general seem to
outweigh the risks.
11 12
Increased number of electrodes and longer dur-
ation of monitoring has been shown to be asso-
ciated with increased frequency of adverse events.
13
Other aspects not explored include age and medi-
cation. Higher age was shown to be associated with
an increased risk for complications at epilepsy
surgery in an earlier Swedish national study
10
and,
therefore, it would be of interest to investigate
whether the risk of complications related to inva-
sive monitoring is also age related. Valproate treat-
ment may induce thrombocytopenia which seems
to be dose dependent with a negative correlation
between valproate trough levels and platelet
counts.
14
Although several studies have found no
indication that patients on valproate treatment are
at an increased risk of surgical bleeding complica-
tions,
15 16
there is a worry about the possible risk,
and some epilepsy surgeons do not operate patients
who are on valproate treatment.
The aim of the current study was to analyse data
from the prospective population-based Swedish
National Epilepsy Surgery Register 1996–2010, in
order to describe the complications related to pre-
operative invasive investigations with intracranial
electrodes. Secondary aims were to explore if the
risk of complications is age related, if there was a
Hedegärd E, et al.J Neurol Neurosurg Psychiatry 2013;0:1–5. doi:10.1136/jnnp-2013-306465 1
Epilepsy
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higher risk of haemorrhagic complications in patients who were
treated with valproate, and whether complications occurring
during invasive monitoring is a risk factor for complications at
therapeutic surgery.
PATIENTS AND METHODS
Every epilepsy surgery procedure in Sweden is reported to the
Swedish National Epilepsy Surgery Register. The register
includes data on all patients who have been operated in Sweden
since 1990. It was initiated by the Swedish Board of Health and
Welfare as a quality control register, and is controlled by the
Swedish Data Inspection Board. All patients whose data are
included in the register have given their informed consent. The
validity of the data collected from the centres is regularly
checked by intrinsic checkpoints within the database and by
external revision. Two epilepsy nurses visit the six centres regu-
larly and compare the data entered into the central database
with the original data from the patient files for a random yearly
sample of around 25% of the patients operated at each centre.
The items controlled in this external revision include side and
site of operation, complications, main histopathological findings
and seizure outcome at the two-year follow-up. So far, there
have been no mismatches in the reporting on any of these
central items. The Regional Board of Medical Ethics at the
University of Gothenburg considered this study a quality control
study not necessitating informed consent for research.
In this study, we have analysed complications after invasive
EEG monitoring in all patients who, prior to surgery, underwent
investigations with subdural strips or grids, intracerebral depth
electrodes, foramen ovale electrodes or epidural electrodes from
January 1996 to December 2010. (During this time period,
Stereo-EEG (SEEG) was not performed in Sweden, the depth
electrodes used were freely placed most often in conjunction
with grid electrodes). Two or more electrode types were often
combined, and when reporting complications in relation to elec-
trode type the most complication-prone electrode type has
been accounted for. The register does, however, not provide
information on the number of electrodes and the duration of
monitoring.
Complications are reported as major or minor to the register,
and the type of complication is commented upon. Minor com-
plications are defined as those that resolve within 3 months,
while major complications affect activities of daily living and
last longer than 3 months. Major complications also include any
significant neurological deficits, even if they do not affect activ-
ities of daily living.
10
The antiepileptic drug treatment at the presurgical investiga-
tion is reported, but not the dosage. The Swedish National
Epilepsy Surgery register does not contain information on
laboratory variables, such as trough levels of antiepileptic drugs
or platelet counts.
Descriptive statistics were used. For comparison between two
groups, Fisher’s Exact test was used for dichotomous variables.
For descriptive purposes ORs with corresponding CIs were cal-
culated. All tests were two-tailed and conducted at 0.05 signifi-
cance level.
RESULTS
Between 1 January 1996 and 31 December 2010, 865 patients
underwent therapeutic surgical procedures. Seven hundred and
ninety-eight of the operations were resections: 523 were tem-
poral lobe resections (TLR) and 142 were frontal lobe resections
(FLR). There were 44 parietal lobe resections (PLR), 27 occipital
lobe resections (OLR), 19 multilobar resections (MLR) and 43
hemispherectomies. Two hundred and seventy-six of the 865
patients (32%) underwent diagnostic intracranial monitoring
with invasive electrodes prior to the therapeutic surgical proced-
ure. Two hundred and sixty-four of them had a resective proced-
ure later, and there were eight multiple subpial trans-sections,
three callosotomies and one exploration. Forty three per cent
(n=61) of the patients who eventually had an FLR were inva-
sively monitored, versus 30% (n=156) of the patients who had a
TLR, 57% of the patients who had a PLR, 30% of the patients
who had an OLR, 63% of the patients who had an MLR and 5%
of the patients who had a hemispherectomy.
Patient age at surgery ranged from two years to 58 years
(median 26 years), 134 (48.6%) were female and 142 (51.4%)
were male. For five patients, data on complications to the inva-
sive investigation were missing, which is why complication data
are reported for 271 patients. For another five patients, data on
electrode type was missing, hence, the analysis of electrode type
related to surgical complications is limited to 271 patients.
There was no surgical mortality in this series. Also, there
were no major complications. Minor complications occurred in
13 of 271 cases (4.8%) (table 1).
Haematomas were most common, associated with a 3.7% risk
(n=10). Of these, seven (2.6%) were subdural haematomas and
three were epidural haematomas (1.1%). Two patients suffered
from wound infections and one from electrode dislocation,
representing a complication rate of 0.7 and 0.4%. Individual
patient data for all complications occurring during intracranial
monitoring are given in table 2.
Ten per cent (n=6) of the 61 patients who were investigated
for an FLR and 4% (n=6) of the 156 patients investigated for a
TLR suffered from complications from the invasive electrode
monitoring. In the group of patients who had complications,
five out of the six who had frontally located electrodes had a
subdural haematoma. Among the patients with complications
from temporally located electrodes, the complication types were
more varied. There was a slight, non-significant difference in
complication rate between female (3.9%, n=5) and male
patients (5.7%, n=8).
Among the 108 patients who were monitored with subdural
grids, eight (7.4%) suffered from complications, mostly haema-
tomas. As shown in table 3, grids had the highest complication
rate, followed by intracerebral depth electrodes. Two patients in
the study had epidural electrodes, and one of them got a sub-
dural haematoma.
When patients were divided into age categories (table 4) there
was a difference between the age groups. Children (age 5–18
years) and young adults (age 18–35 years) had complications in
3.2 and 3.6%, respectively, while 8.3% of adults ≥35 years old
had complications.This difference did not reach statistical sig-
nificance (p=0.12).
Sixty of the 271 patients (22%) in who reports on complica-
tions or not had been registered were treated with valproate at
Table 1 Complications related to intracranial monitoring
Type of complication n (%)
Subdural haematoma 7 (2.6)
Epidural haematoma 3 (1.1)
Wound infection 2 (0.7)
Electrode dislocation 1 (0.4)
Total 13 (4.8)
2 Hedegärd E, et al.J Neurol Neurosurg Psychiatry 2013;0:1–5. doi:10.1136/jnnp-2013-306465
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the time of presurgical investigations, alone or in combination
with other antiepileptic drugs. Three of the 60 patients on val-
proate had a bleeding during invasive monitoring (5%) com-
pared with seven of the 211 patients who were not treated with
valproate (3.3%). Treatment with valproate and having a bleed-
ing was associated with an OR of 1.53 (95% CI 0.38 to 6.12)
compared to having a bleeding and not being treated with val-
proate. This association was, however, not significant as shown
by the wide CI including 1.
In the whole Swedish series of 865 therapeutic surgeries
1996–2010, there were 26 major complications (3%).
17
A post
hoc analysis of a possible relationship between having a compli-
cation during invasive monitoring and at surgery was per-
formed. Two of 13 patients (15%) who had a complication at
the invasive monitoring in addition also suffered a major com-
plication related to the therapeutic procedure, compared to 24/
852 (3%) patients who had a complication only at therapeutic
surgery. Having a complication during invasive monitoring was
associated with a significant OR of 6.27 (CI 1.32 to 29.9) of
also having a complication at therapeutic surgery compared to
the risk of having a complication only at surgery. There was no
relationship between the kind of complication (bleeding or
other) at the one or the other procedure.
DISCUSSION
In this series, the rate of haemorrhagic complications (3.6% of
the patients) was comparable with that reported in a recent sys-
tematic review concerning adverse events related to invasive
EEG monitoring with subdural grid electrodes which identified
21 studies including 2542 patients.
13
In this review, the mean pooled prevalence of haematomas
was 4%. The development of subdural haematoma was the most
common type of complication (2.6%) in our series, more than
half the complications were in this category (n=7). The preva-
lence of subdural haematomas varies widely in the literature and
is reported to be common in some studies, whereas, other
groups report no subdural haematomas at all in their series. In
the abovementioned review, subdural haematomas were docu-
mented in 41 of 2356 patients (pooled prevalence 1.7%).
13
Three (1.1%) of our patients developed epidural haematomas
during the invasive EEG monitoring. This is slightly higher than
the 0.6% reported by Arya et al.
13
Even higher rates have been
reported by Hamer et al (2.5%),
6
while several studies report
no epidural haematomas at all.
18–20
Two (0.7%) of the patients in our study had wound infec-
tions, whereas, there were no intracranial infections. This is a
low number compared to other studies. In the review by Arya
et al, infections emerged as the most common type of complica-
tion with a pooled prevalence of 5.3% (2.3% neurologic infec-
tions and 3.0% superficial infections).
13
Some series also have
significantly higher infection rates.
921
In one prospective study,
the infection rate was shown to increase if more than 100 elec-
trode contacts were used, if more than ten electrode cables were
present, or if electrodes remained implanted for more than
14 days.
22
Since the Swedish National Epilepsy Surgery Register
does not contain data on number of electrode contacts or days,
we were not able to analyse the impact of these factors in our
series. We hypothesise that one reason we do not have any bone
flap or deep infections may be attributed to short surgical
Table 4 Age and complications
Age (years) Patients (n) Complications n (%)
≥2–<5 9 0
≥5–<18 84 3 (3.6)
≥18–<35 94 3 (3.2)
≥35 84 7 (8.3)
Total 271 13
Table 3 Electrode types and complications
Type of invasive
electrodes* n (%)
Complications per
electrode type n (%) Type
Grids 108 (40.5) 8 (7.4) 6 SH/2 EH
Intracerebral depth 14 (5.2) 1 (7.1) 1 D
Foramen ovale 9 (3.4) 0 –
Epidural 2 (0.7) 1 (50) 1 SH
Strips only 134 (50.2) 3 (2.2) 1 EH/2 I
Electrode type alone or in combination, most complication prone first.
*Counted per electrode type.
D, electrode dislocation; EH, epidural haematoma; I, infection; SH, subdural
haematoma.
Table 2 Individual complications occurring during intracranial monitoring
Patient; gender
(age–years) Resection type Electrode type Complication type Comment in the register
Female (13) RFLR Strips+grids Subdural haematoma Haematoma under the grid (evacuated)
Male (14) RFLR Strips+grids Subdural haematoma Haematoma under the grid (evacuated)
Male (16) LTLR Epidural Subdural haematoma No comment
Male (18) LFLR Grids Subdural haematoma Haematoma under the grid (evacuated)
Male (20) LFLR Strips+grids Subdural haematoma Haematoma under the grid
Female (34) RTLR Strips+intracerebral Electrode dislocation A subdural strip electrode was dislocated intraparenchymally
Male (36) LTLR Strips Infection Wound infection
Female (36) RFLR Grids Subdural haematoma Haematoma under the grid
Male (39) LTLR Strips+grids+intracerebral Epidural haematoma Epidural haematoma after implantation of grids (evacuated)
Male (40) MST Strips Epidural haematoma Epidural hematoma in connexion with electrode implantation (evacuated)
Female (42) LTLR Strips+grids Subdural haematoma Haematoma under the grid
Female (44) RTLR Strips Infection Wound infection
Male (56) LFLR Grids Epidural haematoma Epidural haematoma (evacuated)
LFLR, left frontal lobe resection; LTLR, left temporal lobe resection MST, multiple subpial trans-section; RFLR, right frontal lobe resection RTLR, right temporal lobe resection.
Hedegärd E, et al.J Neurol Neurosurg Psychiatry 2013;0:1–5. doi:10.1136/jnnp-2013-306465 3
Epilepsy
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time
23
since we, in general, use fewer grids than reported from
many centres in complication series.
In our series, grid electrodes caused more complications than
other types of electrodes, as eight of 13 affected patients had grid
electrodes alone or in combination with other electrode types.
This correlation between subdural grids and complications has
also been shown by other groups.
424
The reasons for this
increased risk are unclear but could be mechanical or haemo-
dynamic (the grid disturbing the CSF circulation). Whether the
addition of strips to a subdural grid recording increases the risk
of complications cannot be excluded, although strips per se have
a low complication rate. Patients who are investigated for frontal
lobe seizure onset tend to have more grid electrodes than other
patients. This group of patients also suffered from complications
more often than other groups in our series, nearly 10% (6 out of
61), and all were haematomas. Next in line were the patients
investigated for temporal lobe epilepsy, almost 4% (6 out of 156)
had complications. We assume that the high rate of haemorrhagic
complication in patients with frontal lobe seizures was related to
the more common use of grids.
There was a (non-significant) trend towards higher risk for
complications in patients who were 35 years or more in our
series. The association between complications and age has previ-
ously been documented in relation to invasive monitoring,
resective epilepsy surgery procedures and other neurosurgical
procedures, and has been discussed in terms of increasing tissue
fragility and affection of the cerebrovascular system with
increasing age.
61025
On the other hand, Blauwblomme et al
studied adverse events related to invasive EEG monitoring in
children and found a very high complication rate, almost half
the patients suffered from some kind of complication. This can
partly be explained by the fact that in this series a wide range of
adverse events was considered as complications, for example,
cerebrospinal leakage.
9
Minor adverse events such as headache,
nausea, light fever and tiredness during the first postoperative
days can be associated with the implantation of subdural electro-
des, but most surgeons consider them as expected effects of the
implantation and they are rarely documented.
In the post hoc exploration of a possible relationship between
complications during invasive monitoring and at surgery it was
notable that two of the 13 patients with complications in our
study also suffered from major complications after the thera-
peutic resection.
17
Since this association was not explained by
bleedings, some other vulnerability may be at play, for which we
presently have no explanation. In order to verify and elucidate
this finding, prospective multicentre studies of complications
during invasive monitoring and in relation to resective surgery,
collecting more detailed patient data is needed.
There was no significant association between valproate treat-
ment and bleeding complications during invasive monitoring
and, therefore, there is no support for the notion that valproate
treatment is an important risk factor for bleedings. However,
the OR of 1.53 implies that there is a small increase in risk and
it would be valuable if this could be further studied in larger
samples preferably with data on valproate dosage, trough levels
and platelet counts. In one large single centre study, the risk of
bleedings requiring acute decompression was shown not to be
related to the surgical learning curve, and so, not to diminish
over time.
4
The importance of minimising such potentially life-
threatening complications during presurgical investigations
cannot be overstated.
Five deaths directly related to subdural grid implantation
were documented in the systematic review.
13
This does not,
however, cover complications related to depth electrodes. In
general, complications have been reported to be less common
with depth electrodes than with subdural grids,
45726–29
but at
least two fatalities have been reported with SEEG record-
ings.
30 31
Also, Engel et al early on reported two deaths from
intracerebral haemorrhage caused by depth electrodes.
32
An important issue when striving to lower the risk of serious
complications related to invasive monitoring is surveillance. It is
clear from the literature that some reported deaths have been
related to lack of 24 h professional surveillance.
33
While serious
complications cannot totally be avoided, their effects may be
minimised with rapid intervention such as acute decompression.
In our series, all complications were considered minor only
because there were no permanent sequels. However, the most
frequent complications were potentially dangerous subdural and
epidural haematomas. The four Swedish centres in which sub-
dural grids are used all have personalised 24 h surveillance of
those patients and have, therefore, managed to act rapidly in
case of complications.
The spectrum of definitions and scales makes it difficult to
compare studies and, therefore, reporting only percentages is
not very meaningful. The main issues are study methodology on
the one hand, and the definitions of complications on the other.
Most studies are single-centre retrospective studies, while a few
studies analyse prospectively recorded data.
92224
It would be
valuable if an agreement could be reached on how to report
complications associated with invasive EEG monitoring, and
agree about what is to be considered a complication and what
could rather be described as a more or less expected adverse
event. In the present study, we have not considered transient
CSF leakage, fever and headache as complications, as all these
commonly occur after implantation of intracranial electrodes.
Neither have we had as a routine to report small asymptomatic
subdural haematomas. We acknowledge that this is a limitation
of the study, and are aware that it leads more to a ‘top of the
iceberg’reporting, but we capture symptomatic complications
and especially all those necessitating interventions. Another limi-
tation of the study is that the register does not contain informa-
tion on the number of electrodes and duration of invasive
monitoring, and these variables could, therefore, not be related
to the risk of complications.
The main strength of the study is the prospective collection of
population-based data in a large national series. Also, our exter-
nal quality control ensures that the data has been correctly
entered from the patient files into the register.
CONCLUSION
In this prospective population-based epilepsy surgery series, the
most common complications were haematomas, and subdural
grids carried the highest risk of complications. Close supervision
and rapid interventions led to avoidance of permanent morbid-
ity. Whether the slightly increased risk of haematomas with
valproate treatment is clinically relevant needs further investiga-
tion, as does the finding of an increased risk for complications
at epilepsy surgery for patients who had a complication during
invasive monitoring.
There is a need for consensus on how to report complications
related to invasive monitoring in order to provide patients with
adequate information on risks.
Acknowledgements The authors thank Aldina Pivodic for help with the statistical
analyses, and the steering committee of the Swedish National Epilepsy Surgery
Register, and all the Swedish epilepsy surgery teams (in Gothenburg, Linköping,
Lund, Stockholm, Umeå, Uppsala) whose contributions to the register are a
prerequisite for national population-based studies.
4 Hedegärd E, et al.J Neurol Neurosurg Psychiatry 2013;0:1–5. doi:10.1136/jnnp-2013-306465
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Contributors EH analysed the data and drafted the manuscript. JB analysed data,
searched the literature and revised the manuscript. AE analysed data, performed the
statistical analysis and revised the manuscript. BR is responsible for the acquisition
of data, analysed data and revised the manuscript. RF is responsible for the
acquisition of data, and revised the manuscript. KM designed the study, supervised
the analysis and wrote the manuscript. All authors have approved the final version.
Funding The study was funded by grants from the Swedish Research Council grant
number 521–2011-169 and the Sahlgrenska Academy at Gothenburg University
through the LUA/ALF agreement grant number ALFGBG137431. The funding bodies
had no role in the study design; in the collection, analysis and interpretation of
data; in the writing of the report; and in the decision to submit the paper for
publication.
Competing interests None.
Ethics approval The Regional Board of Medical Ethics at the University of
Gothenburg.
Provenance and peer review Not commissioned; externally peer reviewed.
Open Access This is an Open Access article distributed in accordance with the
Creative Commons Attribution Non Commercial (CC BY-NC 3.0) license, which
permits others to distribute, remix, adapt, build upon this work non-commercially,
and license their derivative works on different terms, provided the original work is
properly cited and the use is non-commercial. See: http://creativecommons.org/
licenses/by-nc/3.0/
REFERENCES
1 Schuele SU, Luders HO. Intractable epilepsy: management and therapeutic
alternatives. Lancet Neurol 2008;7:514–24.
2 Spencer S, Huh L. Outcomes of epilepsy surgery in adults and children. Lancet
Neurol 2008;7:525–37.
3 Wiebe S, Blume WT, Girvin JP, et al. Effectiveness, efficiency of surgery for temporal
lobe epilepsy study G. A randomized, controlled trial of surgery for temporal-lobe
epilepsy. N Engl J Med 2001;345:311–18.
4 Wellmer J, von der Groeben F, Klarmann U, et al. Risks and benefits of invasive
epilepsy surgery workup with implanted subdural and depth electrodes. Epilepsia
2012;53:1322–32.
5 Ross DA, Brunberg JA, Drury I, et al. Intracerebral depth electrode monitoring in
partial epilepsy: the morbidity and efficacy of placement using magnetic resonance
image-guided stereotactic surgery. Neurosurgery 1996;39:327–33; discussion 33–4.
6 Hamer HM, Morris HH, Mascha EJ, et al. Complications of invasive video-EEG
monitoring with subdural grid electrodes. Neurology 2002;58:97–103.
7 BehrensE, Schramm J, Zentner J, et al.Surgicalandneurologicalcomplications in a series
of708epilepsy surgery procedures.Neurosurgery1997;41:1–9; discussion -10.
8 Musleh W, Yassari R, Hecox K, et al. Low incidence of subdural grid-related
complications in prolonged pediatric EEG monitoring. Pediatr Neurosurg
2006;42:284–7.
9 Blauwblomme T, Ternier J, Romero C, et al. Adverse events occurring during
invasive electroencephalogram recordings in children. Neurosurgery 2011;69(2
Suppl Operative):169–75; discussion ons75.
10 Rydenhag B, Silander HC. Complications of epilepsy surgery after 654 procedures in
Sweden, September 1990–1995: a multicenter study based on the Swedish
National Epilepsy Surgery Register. Neurosurgery 2001;49:51–6; discussion 6–7.
11 Bekelis K, Radwan TA, Desai A, et al. Subdural interhemispheric grid electrodes for
intracranial epilepsy monitoring: feasibility, safety, and utility: clinical article.
J Neurosurg 2012;117:1182–8.
12 Burneo JG, Steven DA, McLachlan RS, et al. Morbidity associated with the use of
intracranial electrodes for epilepsy surgery. Can J Neurol Sci 2006;33:223–7.
13 Arya R, Mangano FT, Horn PS, et al. Adverse events related to extraoperative
invasive EEG monitoring with subdural grid electrodes: a systematic review and
meta-analysis. Epilepsia 2013;54:828–39.
14 Nasreddine W, Beydoun A. Valproate-induced thrombocytopenia: a prospective
monotherapy study. Epilepsia 2008;49:438–45.
15 Anderson GD, Lin YX, Berge C, et al. Absence of bleeding complications in patients
undergoing cortical surgery while receiving valproate treatment. J Neurosurg
1997;87:252–6.
16 Ward MM, Barbaro NM, Laxer KD, et al. Preoperative valproate administration
does not increase blood loss during temporal lobectomy. Epilepsia
1996;37:98–101.
17 Bjellvi J, Edelvik A, Ekstedt G, et al. Complications of epilepsy surgery in Sweden
1996–2010: results from the Swedish National Epilepsy Surgery Register. Epilepsia
2012;53(Suppl 5):181.
18 Bauman JA, Feoli E, Romanelli P, et al. Multistage epilepsy surgery: safety, efficacy,
and utility of a novel approach in pediatric extratemporal epilepsy. Neurosurgery
2005;56:318–34.
19 Onal C, Otsubo H, Araki T, et al.Complications of invasive subdural grid monitoring
in children with epilepsy. J Neurosurg 2003;98:1017–26.
20 Swartz BE, Rich JR, Dwan PS, et al. The safety and efficacy of chronically implanted
subdural electrodes: a prospective study. Surg Neurol 1996;46:87–93.
21 Simon SL, Telfeian A, Duhaime AC. Complications of invasive monitoring used in
intractable pediatric epilepsy. Pediatr Neurosurg 2003;38:47–52.
22 Wiggins GC, Elisevich K, Smith BJ. Morbidity and infection in combined subdural
grid and strip electrode investigation for intractable epilepsy. Epilepsy Res
1999;37:73–80.
23 Korinek AM, Golmard JL, Elcheick A, et al. Risk factors for neurosurgical site
infections after craniotomy: a critical reappraisal of antibiotic prophylaxis on 4,578
patients. J Neurosurg 2005;19:155–62.
24 Vale FL, Pollock G, Dionisio J, et al. Outcome and complications of chronically
implanted subdural electrodes for the treatment of medically resistant epilepsy.
Clin Neurol Neurosurg 2013;115:985–90.
25 Boviatsis EJ, Bouras TI, Kouyialis AT, et al. Impact of age on complications and
outcome in meningioma surgery. Surg Neurol 2007;68:407–11; discussion 11.
26 Bekelis K, Desai A, Kotlyar A, et al. Occipitotemporal hippocampal depth electrodes
in intracranial epilepsy monitoring: safety and utility. J Neurosurg
2013;118:345–52.
27 Fernandez G, Hufnagel A, Van Roost D, et al. Safety of intrahippocampal depth
electrodes for presurgical evaluation of patients with intractable epilepsy. Epilepsia
1997;38:922–9.
28 Ozlen F, Asan Z, Tanriverdi T, et al. Surgical morbidity of invasive monitoring in
epilepsy surgery: an experience from a single institution. Turk Neurosurg
2010;20:364–72.
29 Sansur CA, Frysinger RC, Pouratian N, et al. Incidence of symptomatic hemorrhage
after stereotactic electrode placement. J Neurosurg 2007;107:998–1003.
30 Cossu M, Schiariti M, Francione S, et al. Stereoelectroencephalography in the
presurgical evaluation of focal epilepsy in infancy and early childhood. J Neurosurg
Pediatr 2012;9:290–300.
31 Guenot M, Isnard J, Ryvlin P, et al. Neurophysiological monitoring for epilepsy
surgery: the Talairach SEEG method. StereoElectroEncephaloGraphy. Indications,
results, complications and therapeutic applications in a series of 100 consecutive
cases. Stereotact Funct Neurosurg 2001;77:29–32.
32 Engel J Jr, Crandall P, Rausch R. The partial epilepsies. In: Rosenberg R,
Grossman R, Schochet S, Heinz E, Willis W, eds. The clinical neurosciences.
New York: Churchill Livingstone, 1983:1349.
33 Wong CH, Birkett J, Byth K, et al. Risk factors for complications during intracranial
electrode recording in presurgical evaluation of drug resistant partial epilepsy. Acta
Neurochir (Wien) 2009;151:37–50.
Hedegärd E, et al.J Neurol Neurosurg Psychiatry 2013;0:1–5. doi:10.1136/jnnp-2013-306465 5
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published online November 29, 2013J Neurol Neurosurg Psychiatry
Emelie Hedegärd, Johan Bjellvi, Anna Edelvik, et al.
observational study
a prospective population-based electrodes:workup with subdural and depth
Complications to invasive epilepsy surgery
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