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Complications to invasive epilepsy surgery workup with subdural and depth electrodes: A prospective population-based observational study

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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. 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. 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. 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.
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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 dene 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 19962010.
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 signicant 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 nding 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 signicant reduction of
seizure frequency in the majority of operated
patients.
13
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 benets 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 denitions of
complications and to study methodology (eg, if
data are obtained retrospectively or prospectively).
Different classications 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 benets 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 19962010, 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;0:15. doi:10.1136/jnnp-2013-306465 1
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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 les 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 ndings
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 dened 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
signicant neurological decits, 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, Fishers 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 signi-
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 ve patients, data on complications to the inva-
sive investigation were missing, which is why complication data
are reported for 271 patients. For another ve 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,
ve 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-signicant 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 518
years) and young adults (age 1835 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-
nicance (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;0:15. 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 signicant as shown
by the wide CI including 1.
In the whole Swedish series of 865 therapeutic surgeries
19962010, 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 signicant 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 identied
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.
1820
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% supercial infections).
13
Some series also have
signicantly 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
ap 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
(ageyears) 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;0:15. doi:10.1136/jnnp-2013-306465 3
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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-signicant) 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 rst 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 nding, prospective multicentre studies of complications
during invasive monitoring and in relation to resective surgery,
collecting more detailed patient data is needed.
There was no signicant 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,
4572629
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 denitions and scales makes it difcult to
compare studies and, therefore, reporting only percentages is
not very meaningful. The main issues are study methodology on
the one hand, and the denitions 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
icebergreporting, 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 les 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 nding 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;0:15. 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 nal version.
Funding The study was funded by grants from the Swedish Research Council grant
number 5212011-169 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/
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Hedegärd E, et al.J Neurol Neurosurg Psychiatry 2013;0:15. doi:10.1136/jnnp-2013-306465 5
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... Relevant hemorrhagic complications that led to early termination of monitoring or required surgical intervention in our series occurred significantly more frequently with SDE explorations (SDE 9.9%, DE 0.3%, p < 0.05%). In other studies, one-third to one-half of all patients with bleeding complications required hematoma evacuation [13][14][15]. The meta-analysis by Arya et al. [5] reported a lower rate of intracranial hemorrhage caused by SDE examinations (pooled prevalence of 4.0%, 1.3% were symptomatic or required surgical intervention). ...
... A review by Mullin and colleagues reported an overall prevalence of infections in DE-only explorations of 0.8% [12]. In contrast, few studies report lower infection rates with subdural grids or strips (0.7-1.1%) [13,14]. In our study, neither type of implantation resulted in a relevant number of infections. ...
... Some studies show that an increased number of electrodes (for both SDE and DE) is associated with an increased incidence of adverse events during invasive monitoring [2,14,19,22]. In particular, an increased risk of infection [7,11,19,22] but also a more frequent development of cerebral edema and other complications [7,14,19,22] have been reported, whereas other series could not confirm this association [4,9,15]. ...
Article
Purpose: To analyze the safety profile of subdural and depth electrode implantation in a large monocentric cohort of patients of all ages undergoing intracranial EEG exploration because of drug resistant focal epilepsy diagnosed and implanted by a constant team of epileptologists and neurosurgeons. Methods: We retrospectively analyzed data from 452 implantations in 420 patients undergoing invasive presurgical evaluation at the Freiburg Epilepsy Center from 1999 to 2019 (n = 160 subdural electrodes, n = 156 depth electrodes and n = 136 combination of both approaches). Complications were classified as hemorrhage with or without clinical manifestations, infection-associated and other complications. Furthermore, possible risk factors (age, duration of invasive monitoring, number of electrode contacts used) and changes in complication rates during the study period were analyzed. Results: The most frequent complications in both implantation groups were hemorrhages. Subdural electrode explorations caused significantly more symptomatic hemorrhages and required more operative interventions (SDE 9.9%, DE 0.3%, p < 0.05). Hemorrhage risk was higher for grids with 64 contacts than for smaller grids (p < 0.05). The infection rate was very low (0,2%). A transient neurological deficit occurred in 8.8% of all implantations and persisted for at least 3 months in 1.3%. Transient, but not persistent neurological deficits were more common in patients with implanted subdural electrodes than in the depth electrode group. Conclusion: The use of subdural electrodes was associated with a higher risk of hemorrhage and transient neurological symptoms. However persistent deficits were rare with either approach, demonstrating that intracranial investigations using either subdural electrodes or depth electrodes carry acceptable risks in patients with drug-resistant focal epilepsy.
... Especially in those cases of pharmacoresistant epilepsy, invasive EEG is a wellestablished part of presurgical diagnostics [28,44]. In this way, invasive diagnostics with depth and/or subdural grid electrodes can be utilized, on the one hand, to identify and localize the epileptogenic focus, with its boundaries not necessarily defined anatomically or easily seen on a macroscopic level and, on the other hand, to evaluate the involvement of close-by eloquent cortical areas [24,29]. ...
Article
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Background: Epilepsy surgery for extratemporal lobe epilepsy (ETLE) is challenging, particularly when MRI findings are non-lesional and seizure patterns are complex. Invasive diagnostic techniques are crucial for accurately identifying the epileptogenic zone and its relationship with surrounding functional tissue. Microscope-based augmented reality (AR) support, combined with navigation, may enhance intraoperative orientation, particularly in cases involving subtle or indistinct lesions, thereby improving patient outcomes and safety (e.g., seizure freedom and preservation of neuronal integrity). Therefore, this study was conducted to prove the clinical advantages of microscope-based AR support in ETLE surgery. Methods: We retrospectively analyzed data from ten patients with pharmacoresistant ETLE who underwent invasive diagnostics with depth and/or subdural grid electrodes, followed by resective surgery. AR support was provided via the head-up displays of the operative microscope, with navigation based on automatic intraoperative computed tomography (iCT)-based registration. The surgical plan included the suspected epileptogenic lesion, electrode positions, and relevant surrounding functional structures, all of which were visualized intraoperatively. Results: Six patients reported complete seizure freedom following surgery (ILAE 1), one patient was seizure-free at the 2-year follow-up, and one patient experienced only auras (ILAE 2). Two patients developed transient neurological deficits that resolved shortly after surgery. Conclusions: Microscope-based AR support enhanced intraoperative orientation in all cases, contributing to improved patient outcomes and safety. It was highly valued by experienced surgeons and as a training tool for less experienced practitioners.
... 7 As for intracranial EEGs, higher risks of complications and hemorrhage brought the need for a lower nurse-to-patient ratio. 2,19 Our survey mirrors previous findings on staff-to-patient ratios in the 2016 Canadian survey: most EMUs employed a nurse-topatient ratio of one to four or less and modified the ratio for invasive monitoring. No changes in this ratio were reported for daytime, nighttime, days of the week, and pediatric versus adult units in the 2016 survey. ...
Article
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Background: Guidelines on epilepsy monitoring unit (EMU) standards have been recently published. We aimed to survey Canadian EMUs to describe the landscape of safety practices and compare these to the recommendations from the new guidelines. Methods: A 34-item survey was created by compiling questions on EMU structure, patient monitoring, equipment, personnel, standardized protocol use, and use of injury prevention tools. The questionnaire was distributed online to 24 Canadian hospital centers performing video-EEG monitoring (VEM) in EMUs. Responses were tabulated and descriptively summarized. Results: In total, 26 EMUs responded (100% response rate), 50% of which were adult EMUs. EMUs were on average active for 23.4 years and had on average 3.6 beds. About 81% of respondents reported having a dedicated area for VEM, and 65% reported having designated EMU beds. Although a video monitoring station was available in 96% of EMUs, only 48% of EMUs provided continuous observation of patients (video and/or physical). A total of 65% of EMUs employed continuous heart monitoring. The technologist-to-patient ratio was 1:1-2 in 52% of EMUs during the day. No technologist supervision was most often reported in the evening and at night. Nurse-to-EMU patient ratio was mostly 1:1-4 independently of the time of day. Consent forms were required before admission in 27% of EMUs. Conclusion: Canadian EMUs performed decently in terms of there being dedicated space for VEM, continuous heart monitoring, and adequate nurse-to-patient ratios. Other practices were quite variable, and adjustments should be made on a case-by-case basis to adhere to the latest guidelines.
Chapter
This chapter discusses a patient with pharmacoresistant post-traumatic epilepsy undergoing intracranial monitoring to characterize areas of ictal onset and guide resection. The stages of epileptogenesis in patients with traumatic brain injury are summarized, as well as the critical role of neuroimaging modalities in determining the extent of cerebral injury. We discuss surgical outcomes in this patient population, surgical interventions available, and predictors of outcome. We explain the risks of intracranial monitoring in this patient population. We stress the importance of medication adherence following resective surgery. Furthermore, we enumerate tools for improving medication compliance, including novel technological tools such as gamification. Additionally, we examine the significance of gliosis in the histopathological analyses of patients with epilepsy. Finally, we discuss semiologies including déjà vu, visual phenomena, and unilateral tonic seizures.
Chapter
The core objective of epilepsy surgery is to treat focal epilepsies and their associated networks without inflicting neurological deficits, aiming for seizure freedom or a significant reduction in the frequency of the most disabling seizures, and improving the patients’ and caregivers’ quality of life. This chapter provides an in-depth overview of the various steps involved in epilepsy surgery, from the identification of surgical candidacy to post-operative surgical follow-up.
Article
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Electrocorticogram (ECoG) is an electrophysiological signal that results from the summation of neuronal activity near the cortical surface. To record ECoG signals, the scalp and skull are surgically opened and electrodes are placed on the cortical surface, either epidurally or subdurally. Owing to its improved spatiotemporal resolution and signal quality compared with electroencephalography, it is widely used to diagnose and treat neurological disorders in clinical settings for several decades, despite the invasiveness of ECoG. Recently, ECoG is applied in research to explore brain functions and connectivity, brain‐computer interfaces, and brain‐machine interfaces. In addition to the need for ECoG in neuroscience research, ECoG devices have advanced in terms of materials, fabrication, and function to overcome the limitations of commercially available ECoG arrays. Here, the conventional use of ECoG in clinical medicine, the new applications of ECoG in basic neuroscience research, and the future challenges in translating recent developments in ECoG devices for clinical use are described.
Article
Implantable neuroelectronic interfaces have enabled advances in both fundamental research and treatment of neurological diseases but traditional intracranial depth electrodes require invasive surgery to place and can disrupt neural networks during implantation. We developed an ultrasmall and flexible endovascular neural probe that can be implanted into sub-100-micrometer-scale blood vessels in the brains of rodents without damaging the brain or vasculature. In vivo electrophysiology recording of local field potentials and single-unit spikes have been selectively achieved in the cortex and olfactory bulb. Histology analysis of the tissue interface showed minimal immune response and long-term stability. This platform technology can be readily extended as both research tools and medical devices for the detection and intervention of neurological diseases.
Preprint
Full-text available
Implantable neuroelectronic interfaces have enabled significant advances in both fundamental research and treatment of neurological diseases, yet traditional intracranial depth electrodes require invasive surgery to place and can disrupt the neural networks during implantation. To address these limitations, we have developed an ultra-small and flexible endovascular neural probe that can be implanted into small 100-micron scale blood vessels in the brains of rodents without damaging the brain or vasculature. The structure and mechanical properties of the flexible probes were designed to meet the key constraints for implantation into tortuous blood vessels inaccessible with existing techniques. In vivo electrophysiology recording of local field potentials and single-unit spikes has been selectively achieved in the cortex and the olfactory bulb. Histology analysis of the tissue interface showed minimal immune response and long-term stability. This platform technology can be readily extended as both research tools and medical devices for the detection and intervention of neurological diseases.
Article
Full-text available
In patients with pharmacoresistant focal-onset seizures, invasive presurgical workup can identify epilepsy surgery options when noninvasive workup has failed. Yet, the potential benefit must be balanced with procedure-related risks. This study examines risks associated with the implantation of subdural strip and grid, and intracerebral depth electrodes. Benefit of invasive monitoring is measured by seizure outcomes. Diagnostic procedures made possible by electrode implantation are described. Retrospective evaluation of invasive workups in 242 epilepsy surgery candidates and additional 18 patients with primary brain tumors implanted for mapping only. Complications are scaled in five grades of severity. A regression analysis identifies risk factors for complications. Outcome is classified according to Engel's classification. Complications of any type were documented in 23% of patients, and complications requiring surgical revision in 9%. We did not find permanent morbidity or mortality. Major risk factor for complications was the implantation of grids and the implantation of electrode assemblies comprising strip and grid electrodes. Depth electrodes were significantly correlated with a lower risk. Tumors were not correlated with higher complication rates. Chronic invasive monitoring of 3-40 days allowed seizure detection in 99.2% of patients with epilepsy and additional extensive mapping procedures. Patients with epilepsy with follow-up >24 months (n = 165) had an Engel class 1a outcome in 49.7% if epilepsy surgery was performed, but only 6.3% when surgery was rejected. The benefit of chronic invasive workup outweighs its risks, but complexity of implantations should be kept to a minimum.
Article
Full-text available
The authors report on the use of stereoelectroencephalography (stereo-EEG) in the presurgical electroclinical evaluation of infants and very young children with focal drug-resistant epilepsy. Fifteen patients (9 girls and 6 boys, mean age 34.1 ± 7.3 months, range 21-45 months), potentially candidates to receive surgical treatment for their focal drug-resistant epilepsy, were evaluated using stereo-EEG recording for a detailed definition of the epileptogenic zone. Stereoelectroencephalography was indicated because neuroradiological (brain MRI) and video-EEG data failed to adequately localize the epileptogenic zone. Stereotactic placement of multicontact intracerebral electrodes was preceded by the acquisition of all pertinent anatomical information from structural and functional MRI and from brain angiography, enabling the accurate targeting of desired structures through avascular trajectories. Stereoelectroencephalography monitoring attempted to record habitual seizures; electrical stimulations were performed to induce seizures and for the functional mapping of eloquent areas. Stereoelectroencephalography-guided microsurgery, when indicated, pointed to removal of the epileptogenic zone and seizure control. Brain MRI revealed an anatomical lesion in 13 patients (lobar in 2 cases, multilobar or hemispheric in 11 cases) and was unremarkable in 2 patients. One patient underwent 2 stereo-EEG studies. The arrangement of the intracerebral electrodes was unilateral in all but 1 case. One patient died the day following electrode placement due to massive brain edema and profound hyponatremia of undetermined cause. In 8 cases intracerebral electrical stimulations allowed mapping of functionally critical areas; in 3 other cases that received purposeful placement of electrodes in presumably eloquent areas, no functional response was obtained. Of the 14 patients who completed stereo-EEG monitoring, 1 was excluded from surgery for multifocality of seizures and 13 underwent operations. Postoperatively, 2 patients exhibited an anticipated, permanent motor deficit, 3 experienced a transient motor deficit, and 2 experienced transient worsening of a preexisting motor deficit. Three patients developed a permanent homonymous hemianopia after posterior resections. Histological analysis revealed cortical malformations in 10 cases. Of the 10 patients with a postoperative follow-up of at least 12 months, 6 (60%) were seizure-free (Engel Class Ia), 2 (20%) experienced a significant reduction of seizures (Engel Class II), and 2 (20%) were unchanged (Engel Class IV). The present study indicates that stereo-EEG plays a prominent role in the presurgical evaluation of focal epilepsies also in the first years of life and that it may offer a surgical option in particularly complex cases that would have scarcely benefitted from further medical treatment. Results of stereo-EEG-guided resective surgery were excellent, with 80% of patients exhibiting a substantial improvement in seizures. In consideration of the potentially life-threatening risks of major intracranial surgery in this specific age group, the authors recommend reserving stereo-EEG evaluations for infants with realistic chances of benefiting from surgery.
Article
OBJECTIVE: To present the first national multicenter study on complications after epilepsy surgery procedures to include all epilepsy surgery centers in Sweden: Göteborg, Linköping, Lund, Stockholm, Umeå, and Uppsala. METHODS: Every epilepsy surgery procedure in Sweden is reported to the Swedish National Epilepsy Surgery Register. The report includes relevant social and medical items and complications. A complication is defined as minor if it resolves within 3 months and major if it affects activities of daily living and lasts longer than 3 months. Follow-up data are recorded for 2 years after the operation. Intrinsic checkpoints and external revision validate the register data. RESULTS: During the inclusion period (September 1990–December 1995), 654 surgical procedures were performed (age range, 6 mo–67 yr). Of these, 205 were invasive electrode procedures (182 first investigations and 23 reinvestigations), and 449 were therapeutic procedures (375 first operations and 74 reoperations). After invasive electrode procedures, only minor complications were reported (6.3%). For all 449 therapeutic procedures (including reoperations), minor complications were reported in 8.9% and major complications in 3.1%. Only one major complication was reported in a patient under the age of 35 years. CONCLUSION: This is the first national multicenter study on complications after epilepsy surgery. It demonstrates that these procedures as performed at six different centers in Sweden are safe, but also that risk is related to age. In patients younger than age 35 years, the risk for a major complication after invasive subdural strip electrode investigation and epilepsy surgery is low.
Article
Object of the Study: In some candidates for epilepsy surgery in whom the decision to operate is difficult to make, invasive presurgical investigations, namely depth electrode recordings, may be needed. The SEEG (StereoElectroEncephaloGraphy) method consists of stereotactic orthogonal implantation of depth electrodes (5 to 15, 11 on average). The object of this study is to clarify the indications for SEEG, to expose its complications, and to display its usefulness in terms of surgical strategy and results. Patients and Methods: 100 patients, suffering from drug-resistant epilepsy and selected as candidates for surgical resection, underwent SEEG between 1996 and 2000. A total of 1,118 electrodes were implanted. For each single case, the sites of implantation of the electrodes were chosen in order to determine either the side of the onset of seizures, or the uni- or multilobar feature of them, or a possible operculo-insular propagation from a temporal onset, and also, using direct electrode stimulation, the proximity of speech or motor area. Results: Complications occurred in 5 patients (2 superficial infections, 2 breakages of electrodes, and 1 intracerebral hematoma responsible for death). SEEG was helpful in most (84&percnt;) of the 100 patients to confirm or annul surgical indication, and to adjust the extent of the resection. In some cases (14&percnt;), SEEG allowed to propose a resection that might have been disputable based solely on noninvasive investigation data. For frontal epilepsy, SEEG was crucial in all cases to delineate the extent of resection. Conclusion: SEEG proved to be a relatively safe and a very useful method in ‘difficult’ candidates for epilepsy surgery. In addition, in some cases the implanted electrodes can be used to perform therapeutic RF thermocoagulation of epileptic foci or networks.
Article
Implantation of subdural grids and invasive electroencephalography (EEG) monitoring is important to define the ictal-onset zone and eloquent cortex in selected patients with medically refractory epilepsy. The objective of this systematic review is to summarize data about adverse events related to this procedure. English-language studies published up to July 2012, reporting such adverse events were reviewed. Outcome measures included demographic variables; surgical protocol including number of subdural electrodes implanted per patient, duration of monitoring, antibiotic, and steroid prophylaxis; and adverse events. Twenty-one studies were identified including a total of 2,542 patients. The reported mean number of electrodes per patient and duration of monitoring varied from 52 to 95 and 5 to 17 days, respectively. There is a trend toward more uniform use of antibiotics and steroids in the perioperative period. Neurologic infections (pooled prevalence 2.3%, 95% confidence interval 1.5–3.1), superficial infections (3.0%, 1.9–4.1), intracranial hemorrhage (4.0%, 3.2–4.8), and elevated intracranial pressure (2.4%, 1.5–3.3) were found to be the most common adverse events. Up to 3.5% of patients required additional surgical procedure(s) for management of these adverse events. Increased number of electrodes (≥67) was found to be independently associated with increased incidence of adverse events. Although providing critical information for patients with medically refractory epilepsy, subdural grids implantation and invasive EEG monitoring entails risks of infection, hemorrhage, and elevated intracranial pressure. The prevalence estimates, likely to be conservative due to selective reporting, are expected to be helpful in counseling patients.
Article
Background: Surgery for medically resistant epilepsy is safe and effective. However, when noninvasive techniques are insufficient, then consideration is given to invasive electrocorticography (EcoG). Objective: The aim of the study was to analyze results and complications of subdural electrodes placement in the treatment of intractable epilepsy. Methods: Ninety-one consecutive patients who underwent placement of subdural electrodes (1999-2010) were considered for this study. All patients underwent a standardized pre-operative evaluation. Invasive subdural electrode placement was considered when there were inadequate ictal recordings, there was discordance between EEG and neuroimaging or the epileptogenic zone was localized near eloquent cortex. Results: Resective epilepsy surgery was performed in 70/91 patients (76.9%). Twenty-four out of seventy (34.3%) who underwent surgical resection were seizure-free (CL-I) at last follow-up. A statistical evaluation revealed a very strong trend for patients with positive lesional pre-operative MRI to have improved outcomes compared to normal brain MRI population (p=.028). There were 10 surgical related complications (11%), but no mortality or permanent morbidity. Statistical analysis demonstrated that placement of a subdural grid in any combination was statistically significant (p=.01) for surgical complications. Conclusions: Invasive monitoring is a useful and necessary technique for the surgical treatment of intractable epilepsy. Careful surveillance is required during the monitoring period especially when the patient has undergone large subdural grid placement. A good working hypothesis can minimize complications and achieve better outcomes.
Article
Object: Intracranial monitoring for epilepsy has been proven to enhance diagnostic accuracy and provide localizing information for surgical treatment of intractable seizures. The authors investigated the usefulness of hippocampal depth electrodes in the era of more advanced imaging techniques. Methods: Between 1988 and 2010, 100 patients underwent occipitotemporal hippocampal depth electrode (OHDE) implantation as part of invasive seizure monitoring, and their charts were retrospectively reviewed. The authors' technique involved the stereotactically guided (using the Leksell model G frame) implantation of a 12-contact depth electrode directed along the long axis of the hippocampus, through an occipital twist drill hole. Results: Of the 100 patients (mean age 35.0 years [range 13-58 years], 51% male) who underwent intracranial investigation, 84 underwent resection of the seizure focus. Magnetic resonance imaging revealed mesial temporal sclerosis (MTS) in 27% of patients, showed abnormal findings without MTS in 55% of patients, and showed normal findings in 18% of patients. One patient developed a small asymptomatic occipital hemorrhage around the electrode tract. The use of OHDEs enabled epilepsy resection in 45.7% of patients who eventually underwent standard or selective temporal lobe resection. The hippocampal formation was spared during surgery because data obtained from the depth electrodes showed no or only secondary involvement in 14% of patients with preoperative temporal localization. The use of OHDEs prevented resections in 12% of patients with radiographic evidence of MTS. Eighty-three percent of patients who underwent resection had Engel Class I (68%) or II (15%) outcome at 2 years of follow-up. Conclusions: The use of OHDEs for intracranial epilepsy monitoring has a favorable risk profile, and in the authors' experience it proved to be a valuable component of intracranial investigation. The use of OHDEs can provide the sole evidence for resection of some epileptogenic foci and can also result in hippocampal sparing or prevent likely unsuccessful resection in other patients.
Article
Object: Intracranial monitoring for epilepsy has been proven to enhance diagnostic accuracy and provide localizing information for surgical treatment of intractable seizures. The authors investigated their experience with interhemispheric grid electrodes (IHGEs) to assess the hypothesis that they are feasible, safe, and useful. Methods: Between 1992 and 2010, 50 patients underwent IHGE implantation (curvilinear double-sided 2 × 8 or 3 × 8 grids) as part of arrays for invasive seizure monitoring, and their charts were retrospectively reviewed. Results: Of the 50 patients who underwent intracranial investigation with IHGEs, 38 eventually underwent resection of the seizure focus. These 38 patients had a mean age of 30.7 years (range 11-58 years), and 63% were males. Complications as a result of IHGE implantation consisted of transient leg weakness in 1 patient. Of all the patients who underwent resective surgery, 21 (55.3%) had medial frontal resections, 9 of whom (43%) had normal MRI results. Localization in all of these cases was possible only because of data from IHGEs, and the extent of resection was tailored based on these data. Of the 17 patients (44.7%) who underwent other cortical resections, IHGEs were helpful in excluding medial seizure onset. Twelve patients did not undergo resection because of nonlocalizable or multifocal disease; in 2 patients localization to the motor cortex precluded resection. Seventy-one percent of patients who underwent resection had Engel Class I outcome at the 2-year follow-up. Conclusions: The use of IHGEs in intracranial epilepsy monitoring has a favorable risk profile and in the authors' experience proved to be a valuable component of intracranial investigation, providing the sole evidence for resection of some epileptogenic foci.