Complications of invasive subdural grid monitoring ... - Semantic Scholar

J Neurosurg 98:1017–1026, 2003

Complications of invasive subdural grid monitoring in children with epilepsy ÇAGATAY ÖNAL, M.D., HIROSHI OTSUBO, M.D., TAKASHI ARAKI, M.D., SHIRO CHITOKU, M.D., AYAKO OCHI, M.D., SHELLY WEISS, M.D., WILLIAM LOGAN, M.D., IRENE ELLIOTT, R.N., O. CARTER SNEAD III, M.D., AND JAMES T. RUTKA, M.D., PH.D. Divisions of Neurosurgery and Neurology, The Hospital for Sick Children, The University of Toronto, Ontario, Canada Object. This study was performed to evaluate the complications of invasive subdural grid monitoring during epilepsy surgery in children. Methods. The authors retrospectively reviewed the records of 35 consecutive children with intractable localizationrelated epilepsy who underwent invasive video electroencephalography (EEG) with subdural grid electrodes at The Hospital for Sick Children between 1996 and 2001. After subdural grid monitoring and identification of the epileptic regions, cortical excisions and/or multiple subpial transections (MSTs) were performed. Complications after these procedures were then categorized as either surgical or neurological. There were 17 male and 18 female patients whose mean age was 11.7 years. The duration of epilepsy before surgery ranged from 2 to 17 years (mean 8.3 years). Fifteen children (43%) had previously undergone surgical procedures for epilepsy. The number of electrodes on the grids ranged from 40 to 117 (mean 95). During invasive video EEG, cerebrospinal fluid leaks occurred in seven patients. Also, cerebral edema (five patients), subdural hematoma (five patients), and intracerebral hematoma (three patients) were observed on postprocedural imaging studies but did not require surgical intervention. Hypertrophic scars on the scalp were observed in nine patients. There were three infections, including one case of osteomyelitis and two superficial wound infections. Blood loss and the amounts of subsequent transfusions correlated directly with the size and number of electrodes on the grids (p 0.001). Twenty-eight children derived significant benefit from cortical resections and MSTs, with a more than 50% reduction of seizures and a mean follow-up period of 30 months. Conclusions. The results of this study indicate that carefully selected pediatric patients with intractable epilepsy can benefit from subdural invasive monitoring procedures that entail definite but acceptable risks.

KEY WORDS • subdural electrode grid • invasive monitoring • epilepsy surgery • complication • children

prevalence of epilepsy is reported to be between 4.3 and 9.3 persons per 1000.24 Ninety percent of patients with epilepsy suffer their first seizure in the first two decades of life, and in 10 to 20% of this population the disease is known to be refractory to drug therapy or the patients are affected by the serious side effects of the medications.24,35 Because of this large number of children with refractory epilepsy, and because there is still a significant mortality rate associated with pediatric epilepsy,9,14,15,32 there has been growing interest in providing surgical options for patients whose epilepsy can be localized.1–4,8,10,12,19,21–26,28,31, 36–39,46,49,50 Although there are reports in which noninvasive surgical protocols have been followed with some good results,13,27,45,57 increasingly there has been interest in performing invasive monitoring to identify patients with nonlateral-

T

HE

Abbreviations used in this paper: CSF = cerebrospinal fluid; CT = computerized tomography; EEG = electroencephalography; ICH = intracerebral hematoma; MEG = magnetoencephalography; MR = magnetic resonance; MST = multiple subpial transection; SDH = subdural hematoma.

J. Neurosurg. / Volume 98 / May, 2003

ized epilepsy who could potentially benefit from surgery. In addition to depth electrodes and multiple strip electrodes, which have been the most frequently used invasive monitoring tools, the introduction of large subdural grids for chronic EEG recordings in the 1980s has had a major impact on identifying patients who are eligible for surgery.1–4, 6,7,10,12,17,28,29,31,33,37,39,46,47,50–52,54,56,58,62,66–68 Chronic subdural grid recordings provide the epilepsy treatment team with more accurate delineation of regions of eloquent cortex and epileptogenic foci than do noninvasive strategies or awake craniotomy. The information derived from chronic subdural recordings can then be used to plan an aggressive approach to the epileptogenic focus to maximize favorable outcomes.1,3,7,10,12,16–19,48–53,58,60,61,63–68 Although the focus of most publications on chronic invasive monitoring for epilepsy is understandably on seizure outcome,3–7,10,28,29,31,33,37,46,48,51,56,58,59,61,62,68 the accumulated data on the adverse events associated with subdural grid surgery are still insufficient. There have been a few reports previously that have emphasized the complications of subdural grid monitoring;6,7,29,33,56,58,62 however, none of these studies 1017

Ç. Önal, et al. TABLE 1 Clinical characteristics of 35 children with intractable epilepsy who underwent invasive video EEG monitoring before resection* Case No.

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35

Age (yrs), Sex

Ictal Onset on IVEEG

Grid Location

Location of Resection &/or MSTs

15, M 6, M 13, M 10, M 16, F 11, F 15, F 9, M 12, F 8, M 16, F 14, F 9, F 14, F 18, M 4, M 16, F 10, M 18, F 19, F 18, M 9, M 13, M 2, F 14, F 14, F 7, M 14, M 4, F 6, M 11, F 15, M 4, M 16, F 11, F

rt central lt perisylvian lt frontotemporal lt frontoparietal lt mesiotemporal rt frontoparietal rt frontotemporal rt temporoparietal rt temporoparietal lt perisylvian rt perirolandic rt frontal lt frontoparietal rt occipitotemporal lt frontotemporal rt frontotemporal rt frontal rt occipitotemporal lt frontotemporal rt frontoparietal bilat bilat lt parietooccipital rt central lt parietal lt frontal rt parietooccipital lt central lt parietooccipital lt occipitotemporal lt frontoparietal lt frontotemporal lt temporal rt frontotemporal lt frontal

rt hemisphere lt hemisphere lt hemisphere lt hemisphere lt hemisphere rt hemisphere rt hemisphere rt hemisphere rt hemisphere lt hemisphere rt hemisphere rt hemisphere lt hemisphere rt hemisphere lt hemisphere rt hemisphere rt hemisphere rt hemisphere lt hemisphere rt hemisphere lt hemisphere lt hemisphere lt hemisphere rt hemisphere lt hemisphere lt hemisphere rt hemisphere lt hemisphere lt hemisphere lt hemisphere lt hemisphere lt hemisphere lt hemisphere rt hemisphere lt hemisphere

rt posterosuperior frontal lt temporal, perisylvian lt frontal lt frontal lt temporal rt frontotemporoparietal rt frontal, posterior temporal rt temporoparietal rt temporoparietal lt perisylvian rt perirolandic rt frontal lt frontoparietal rt occipitotemporal lt frontal rt frontotemporal rt frontal rt occipitotemporal lt frontotemporal rt frontoparietal none performed none performed lt occipital, perirolandic rt central lt frontoparietal lt inferior frontal rt parietooccipitofrontal lt frontotemporooccipital lt parietooccipital lt occipitotemporal lt frontotemporoparietal lt frontotemporal lt temporal rt frontoparietotemporal lt frontoparietal

Pathological Findings

astrogliosis cortical dysplasia cortical dysplasia cortical dysplasia cortical dysplasia gliosis gliosis gliosis MTS NA NA gliosis cortical dysplasia MTS cortical dysplasia cortical dysplasia cortical dysplasia gliosis cortical dysplasia gliosis NA NA cortical dysplasia gliosis cortical dysplasia cortical dysplasia MTS Rasmussen syndrome tuberous sclerosis DNET no diagnosis cortical dysplasia gliosis gliosis cortical dysplasia

Outcome†

FU (mos)

I III I II I III II IV II III IV III IV I I III I III I III IV IV IV II II I III IV I I I I I III I

41 45 39 38 28 47 45 37 24 49 60 26 36 26 22 23 29 26 25 25 20 46 25 23 40 21 39 41 57 20 18 18 18 21 18

* DNET = dysembryoplastic neuroepithelial tumor; FU = follow up; IVEEG = invasive video EEG; MTS = mesial temporal sclerosis; NA = not available: resection not performed. † Outcomes were classified according to a modified Engel scale.

has dealt exclusively with the pediatric population. Our aim in writing this report is mainly to address the complications that can arise directly from subdural grid implantation as well as the anticipated or unanticipated adverse events dependent on the natural course of the disease and surgical intervention.

Clinical Material and Methods Patient Population

Thirty-five consecutive children who underwent implantation of large subdural grid electrodes to record invasive video EEG-derived data between June 1996 and June 2001 form the basis of this study. Table 1 describes the patient demographics, ictal onset according to invasive video EEG, grid and resection locations, pathological findings, and seizure outcome data. There were 17 male and 18 female patients, whose ages ranged from 2 to 19 years (mean 11.7 years). The duration of epilepsy ranged from 2 to 17 years (mean 8.3 years). Twenty grids were placed over the left and 15 over the right hemisphere. Thirty-four patients had 1018

contralateral strips (97%) and 17 patients (48%) had depth electrodes inserted. Fifteen children had undergone at least one previous neurosurgical intervention. Of these, five underwent multiple subdural strip insertions for seizure lateralization; six had resections involving at least one lobe, three underwent biopsy procedures, and one had an anterior two-thirds callosotomy. All children had intractable extratemporal epilepsy disrupting their quality of life, with or without temporal lobe localization-related epilepsies. In all patients multiple trials of anticonvulsant therapy had failed. Prior to invasive video EEG monitoring, all children had been evaluated with EEG and video EEG monitoring. Neuroimaging modalities included MR imaging, MEG [18F]fluorodeoxyglucose–positron emission tomography scanning and/or single-photon emission CT scanning. Formal neuropsychological tests were performed on cooperative patients. Wada testing, functional MR imaging, or MEG was used to determine hemispheric language dominance. Subdural Grid Placement

Subdural grids (Ad-Tech Medical Instrument Co., RaJ. Neurosurg. / Volume 98 / May, 2003

Complications of subdural grid monitoring in children

FIG. 1. Upper Left: Intraoperative photograph showing exposure of the hemisphere after craniotomy for subdural grid implantation. Most children underwent large craniotomies for implantation of subdural grids (the mean electrode number in the series was 95). Upper Right: Intraoperative photograph showing a large subdural grid with 105 electrodes. Two temporal depth and one subfrontal strip electrodes are also shown. Lower: Skull x-ray film showing positioning of the subdural grid, subdural strips, and depth electrodes.

cine, WI) were custom-made for each patient by using data from the seizure symptomatology, interictal and ictal scalp EEG recordings, interictal spike sources, and somatosensory evoked fields documented by MEG. Grid size was ultimately determined using three-dimensional MR imaging as previously reported.12 The electrodes were 5 mm in diameter and were embedded in a silastic sheet, with center-tocenter interelectrode distances ranging from 10 to 13 mm. The grids ranged in size from 40 to 117 platinum electrodes (mean 95). In several cases, unilateral subdural electrode strips and depth electrodes were placed to capture ictal data from larger regions of the hemisphere than could be covered by the grid. For grid placement, a generous craniotomy was fashioned, the bone flap was removed, and a large M-shaped dural opening based on the sagittal sinus was made (Fig. 1 upper left). After exposure of the hemisphere, the subdural grid was placed on the cortical surface (Fig. 1 upper right). To prevent displacement, the grid was sutured to the dura. The dura was then closed with large dural grafts, and the bone flap was hinged superiorly. Individual cables were then tunneled separately through the scalp away from the incision, and secured in place with purse-string sutures. Collodion was applied to the exit sites as a sealant; no drains were used. A bulky head dressing was applied.

cuit video EEG monitoring and for extraoperative cortical stimulation of motor, sensory, and language functions while the patient was in the intensive care unit. Any change in the level of consciousness or evolving new neurological deficit was evaluated by CT scanning. Antiepileptic medications were usually reduced and an antibiotic combination of cefotaxime and vancomycin was used during the perioperative period. Grid Removal, Cortical Resection, and MST

After obtaining sufficient data about functional cortex and regions of epileptogenesis, the subdural grid was removed and epileptic regions were resected or treated with MSTs. After an overnight stay in the intensive care unit, the patient was transferred to the ward. Postoperative seizure control was categorized using a modified Engel classification system.18,24,25 Patients in Class I were seizure free postoperatively; those in Class II had occasional seizures postsurgery but less than one per month; those in Class III had a greater than 50% decrease in postoperative seizure frequency; and patients in Class IV had a less than 50% improvement or worsening compared with their preoperative status. Data Analysis

Invasive Video EEG Recording

A plain skull x-ray film and a head CT scan were obtained immediately after surgery to verify grid placement (Fig. 1 lower). Subdural grids were then used for closed-cirJ. Neurosurg. / Volume 98 / May, 2003

Complications during invasive video EEG and after cortical excision were classified as either surgical or neurological. Neurological deficits were further divided into transient or permanent ones; permanent neurological deficits 1019

Ç. Önal, et al. TABLE 2 Adverse events during surgery in children with epilepsy Adverse Event

during grid insertion & IVEEG CSF leak cerebral edema SDH ICH after cortical excision & MST hypertrophied scar phlebitis alopecia along scar bone defect delayed wound healing subgaleal CSF collection wound infection urinary tract infection meningitis ICH osteomyelitis skin necrosis hyponatremia pneumonia

No. of Patients (%)

7 (20) 5 (14) 5 (14) 3 (9) 9 (26) 7 (20) 5 (14) 5 (14) 4 (11) 4 (11) 3 (9) 2 (6) 1 (3) 1 (3) 1 (3) 1 (3) 1 (3) 1 (3)

were defined as those that persisted more than 1 year postsurgery. We performed a univariate analysis by using the Fisher t-test to evaluate differences between factors such as demographics, surgical procedure and seizure outcome. Differences that reached statistical significance were defined as those with a probability value less than 0.05. Results Surgical Complications

The surgical complications that occurred during and after invasive video EEG monitoring, cortical excision, and/or MST are shown in Table 2. Seven patients (20%) had CSF leaks. In four cases the leaks stopped spontaneously within 2 days; however, the other three patients required reinforcing sutures around the electrode cable exit sites. In one patient a prominent subgaleal CSF collection developed, which required placement of a lumbar drain for 5 days. During invasive video EEG monitoring, cerebral edema was noted on neuroimages obtained in five patients (14%). One patient suffered profound brain swelling after grid implantation, which became manifest as the dura was being closed. This patient’s bone flap was left out during the monitoring period. The invasive video EEG monitoring was continued for 5 days, and the bone flap was subsequently replaced at the second stage without difficulty. We detected SDHs in five patients (14%) on CT scans (Fig. 2); none was symptomatic. The SDHs were identified either above the grid (three patients), or under the grid (two patients) (Fig. 3), and were evacuated when the grid was explanted. None of the patients had evidence of blood dyscrasias and none of the SDHs required an additional surgical procedure to that which was planned. We observed ICHs in four patients (11%), with three lesions diagnosed on CT scans, two of which were managed conservatively. Formation of an ICH after MST in an 8-year-old boy with Landau–Kleffner syndrome was diag1020

FIG. 2. Axial CT scan obtained after right cortical resection, demonstrating a small right frontal acute SDH for which no treatment was required.

nosed intraoperatively by using ultrasonography, and the lesion was removed in the same session. The other ICH diagnosed on CT scanning created an epileptogenic focus that subsided after evacuation with the aid of ultrasonography in the second stage of the operation (Fig. 4). No additional surgical procedures were required in the management of the ICHs. The most frequent complication in this series was hypertrophic scar formation (nine patients). Even though complaints about a palpable scar were relatively common, only one patient (3%) needed reconstructive surgery involving placement of a tissue expander, scalp expansion, and scalp flap reconstruction. In five patients (14%) alopecia was a delayed postsurgical complaint. Bone loss was detected in five patients (14%), in four at the sites of burr holes. Wound infection was observed in three children (9%). One of the two superficial wound infections required excision along the incision line when antibiotic agents failed; the other infection was managed conservatively with antibiotics and healed well. The most serious infection in the series was observed in an 11-year-old boy who underwent a right hemispheric craniotomy that was complicated by scalp infection, osteomyelitis, and epidural abscess. Two months postsurgery, a third intervention consisting of reopening of the craniotomy, evacuation and debridement of the epidural abscess, and curettage and internal fixation of the bone flap was performed. Results of wound cultures revealed a Staphylococcus aureus infection that responded to long-term antibiotic therapy. No signs of recurrent infection were detected after 48 months of follow up. One patient (3%) had suspected postoperative meningitis—this was a child with Landau–Kleffner syndrome who was readmitted with headache 2 days after discharge. High-dose intravenous ceftriaxone therapy for was administered for 10 J. Neurosurg. / Volume 98 / May, 2003

Complications of subdural grid monitoring in children

FIG. 3. Intraoperative photograph showing a linear SDH under the grid, which caused partial interference with electrophysiological recordings.

days even though the culture results after lumbar puncture showed no infection. Blood Loss and Blood Transfusion

Table 3 summarizes the data relating to grid size, blood loss, and requirements for transfusion. We monitored patients implanted with subdural grids for 4 to 10 days (mean 5 1.7 days). We inserted subdural strips over the contralateral hemisphere in 34 patients to evaluate contralateral ictal discharges. In 17 patients, we placed additional depth electrodes and subdural strips in the mesial temporal, interhemispheric, or basal regions. Total blood loss during the two-stage operations ranged from 150 to 1250 ml (mean 756 308 ml), and the amount of blood transfused ranged from 175 to 1020 ml (mean 521 368 ml). In 14 patients, the total blood loss was 1000 ml or more. The blood loss in 19 patients with fewer than 100 subdural grid electrodes was 608 282 ml. In 16 patients with 100 or more electrodes, the blood loss was 943 218 ml. Twelve (63%) of 19 patients who had grids with fewer than 100 electrodes required blood transfusion. All 16 patients (46%) with grids having more than 100 electrodes required blood transfusions. Of the 28 patients who received blood transfusions, 12 received them during the first craniotomy, eight during the monitoring period, and eight during the second stage, when resection or MSTs were to be performed. There were no apparent complications related to blood transfusions in this series. Neurological Adverse Events

The neurological deficits related to invasive monitoring in this series are shown in Table 4. The adverse event with the highest documented frequency was hemiparesis. Twenty-four (69%) of 35 patients had mild to moderate postoperative contralateral hemiparesis, which typically resolved within the 1st week after surgery. No permanent hemiparesis was encountered in this series. The second most common neurological deficits were dysphasia and facial weakness, in 18 (51%) and 17 (48%) patients, respectively. Thirteen (37%) of the 35 patients had postoperative visual field defects ranging from minimal field alterations to J. Neurosurg. / Volume 98 / May, 2003

FIG. 4. Axial CT scan obtained in a patient in whom a large right subdural grid and contralateral strip electrodes were implanted. Note the ICH in the right temporal lobe. The presumed mechanism of this hematoma was occlusion of venous outflow by the grid, which led to hemorrhagic infarction.

significant contralateral hemianopsia. All visual field defects were permanent and expected, considering the targeted surgical approach to the epileptic foci. Five patients (14%) experienced an acute postoperative increase in seizures. Seizure Outcome

Follow up ranged from 18 to 60 months (mean 30 13 months). Nineteen patients (54%) achieved good seizure control and were either seizure free (14) or had occasional seizures (five) (Engel Classes I and II; Table 1). Nine patients (26%) had a greater than 50% reduction in seizure frequency (Engel Class III); the remaining seven patients (20%) had residual seizures without improvement (Engel Class IV). In two of these patients, resection or MSTs could not be offered because we failed to localize the ictal onset zone by using invasive video EEG. Results of Statistical Comparisons

On univariate analysis, age, sex, total amounts of blood loss, and blood transfusion were not significantly different between the good seizure outcome (Engel Classes I and II) and poor seizure outcome groups (Engel Classes III and IV). Only the relationship between number of grid electrodes (using grids with 100 electrodes as a reference) and blood loss reached statistical significance (p 0.001). Discussion In recent years, early epilepsy surgery for children has been advocated by many groups.4,10,19,21,22,26,28,31,37–39,42,44,46,50 The main rationale for this trend is the favorable response 1021

Ç. Önal, et al. TABLE 3 Blood loss and transfusion requirements in 35 children who underwent surgery for intractable epilepsy* No. of Electrodes Case No.

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35

MP (days)

4 7 6 4 7 4 4 4 4 4 4 7 9 4 4 7 4 7 4 4 10 4 4 4 4 4 3 4 6 4 8 3 4 7 4

Total

In Grid

108 59 124 112 86 137 127 128 133 98 94 124 122 111 124 118 128 128 124 128 116 123 108 107 116 100 104 99 97 135 113 109 90 120 111

92 40 116 100 70 117 107 104 117 90 79 108 102 95 104 94 96 100 104 116 104 91 88 95 104 100 64 87 78 115 97 93 70 96 93

Subdural Strips

yes yes yes yes yes yes yes yes yes yes yes yes yes yes yes yes yes yes yes yes yes yes yes yes yes no yes yes yes yes yes yes yes yes yes

Depth Electrodes

no no no no yes no yes yes no no no no yes yes yes yes yes yes yes no no no yes no no no no no no yes yes yes yes yes yes

Type of Epilepsy Op

CR, MSTs CR, MSTs CR, MSTs CR, MSTs temp lob & AH CR, MSTs CR, MSTs CR, MSTs CR, MSTs MSTs MSTs CR, MSTs CR, MSTs CR, MSTs front lob CR, MSTs front lob CR, MSTs CR, MSTs CR, MSTs none none CR, MSTs CR, MSTs CR, MSTs CR, MSTs CR, MSTs FTO lob, MSTs CR, MSTs CR, MSTs CR, MSTs CR, MSTs CR, MSTs CR, MSTs CR, MSTs

Blood Loss (ml)

Amount Transfused (ml)

650 150 1050 1100 200 1250 450 1000 1050 760 300 1000 550 500 650 900 500 1100 1000 1100 1000 950 1100 250 800 1000 350 750 400 1000 800 1000 550 800 450

— — 1020 930 — 900 520 615 1000 885 — 580 420 500 850 235 245 1010 910 1020 500 280 1000 — 450 850 — — 475 580 500 990 175 600 200

* AH = amygdalohippocampectomy; CR = cortical resection; front = frontal; FTO = frontotemporooccipital; lob = lobectomy; MP = monitoring period; none = no cortical resection or MSTs performed; temp = temporal; — = no transfusion.

of the child’s brain to cortical resection. After successful epilepsy surgery, the pediatric patient may demonstrate enhanced neurocognitive development because of the elimination or decreased frequency of epileptic discharges. In addition, a benefit is derived in this group from the tapering or cessation of anticonvulsant drugs, many of which lead to significant complications with long-term use.28,37 Despite advances in preoperative imaging modalities such as positron emission tomography, functional MR imaging, and MEG, these imaging methods do not as yet provide an unequivocal localization of the seizure focus.40,41,43, 52,55 Nevertheless, promising results have been reported in carefully selected patients with epilepsy in whom invasive monitoring was used.2,3,10,19,48,49,58,61,64,68 Bruce and Bizzi10 recently reported a success rate of between 80 and 90% in identifying the epileptogenic foci in children in whom invasive monitoring strategies were used. Reports on the complications related to invasive monitoring are far from uniform.11,16,20,49,53,54,61,64,65 With the exception of a few reports specifically on this topic, in which results in the adult population are primarily discussed,3,6,20,29,30,34,56 1022

the adverse effects of invasive monitoring in a series of pediatric patients have not been critically analyzed and reported systematically. In our series, we categorized adverse events caused by subdural grid implantation as either surgical or neurological; the latter were either transient or permanent. For the purposes of this report, emphasis has been placed on the surgical complications related to subdural grid implantation. Many of the adverse events reported in our series were directly related to the surgical site and to the size of the craniotomy. One of the most common complications of invasive subdural grid monitoring is CSF leakage. Adelson, et al.,2 reported on four (13%) of 31 patients with transient CSF leakage through electrode exit sites. These patients were all successfully treated with collodion application and monitoring was continued. In the study by Swartz, et al.,56 19% CSF leakage was reported as an expected adverse event in their series of invasive monitoring procedures. Subgaleal or epidural fluid collection with subsequent surgery for drainage has been reported in some series.28,37 In our series, the incidence of CSF leakage was approximateJ. Neurosurg. / Volume 98 / May, 2003

Complications of subdural grid monitoring in children ly 20%; fortunately, the CSF leaks stopped spontaneously in four of seven patients. To prevent CSF leaks from occurring, we have found that purse-string sutures tied tightly around the electrode cable exit sites and reinforced with collodion work well. None of our patients developed meningitis. Complications such as wound infection, meningitis, osteomyelitis, and epidural abscess formation are also reported in several invasive monitoring series.6,10,19,28,29 In their series of 85 children who underwent invasive monitoring, Bruce and Bizzi10 reported on three patients (4%) who needed bone flap removal because of delayed infection. In their series there were two additional superficial wound infections (2%). In his experience with epidural electrode arrays, Goldring19 reported one bone flap removal without infection. In one of his first patients to undergo invasive monitoring, the bone flap was removed and steam-autoclaved before its insertion during the second procedure; however, aseptic necrosis developed and it had to be removed. Kim, et al.,28 reported on three children with postoperative wound infection, two requiring bone flap removal and the third with meningitis. Two cases of major infection (4%) in 49 patients with 50 subdural grids and/or strips or depth electrodes were reported by Lee, et al.29 One was osteomyelitis necessitating bone flap removal and the other one was a brain abscess requiring stereotactic aspiration. Behrens, et al.,6 reported a 3.5% rate of wound infection in their series. They reported four cases of meningitis during electrode implantation despite negative results on microbial cultures. Uematsu, et al.,58 described two cases of postoperative wound infection (7%) in a series of 28 patients who underwent grid implantation. Morrison, et al.,37 described two superficial wound infections, one sterile abscess, and three bone flap removals requiring late cranioplasties in their pediatric epilepsy experience. Recently, Hamer, et al.,20 reported a 12.1% infection rate in their large series of 187 patients with complications caused by invasive video EEG monitoring. In their series there was a 7.1% meningitis rate and a 3% osteomyelitis rate. With such diverse results in these heterogeneous series, it is hard to reach reliable conclusions regarding the infection rate after invasive monitoring. Nonetheless, our results, in which three patients (9%) had wound infections, one of them accompanying osteomyelitis, are in accordance with those reported previously. The patient with osteomyelitis described here had a large hemicalvarial bone flap that was affixed to the skull with absorbable sutures. This complication occurred early in our series, and we have since changed our method of bone flap replacement to rigid fixation with titanium microplates and screws. We hope that such rigid fixation systems accompanied by the use of prophylactic antibiotics, in our case a third-generation cephalosporin and vancomycin, will help further decrease the rate of surgical infections. A potentially serious problem in patients with implanted grids is cerebral edema. Morrison, et al.,37 reported on one child in their series who died after placement of subdural electrodes. This child went into status epilepticus and died of malignant cerebral edema despite a large frontal lobectomy. In the same article, Morrison, et al., reported on four (8%) of 48 patients with cerebral edema who underwent invasive monitoring and in whom the second-stage operation was performed sooner than planned. Lee, et al.,29 reJ. Neurosurg. / Volume 98 / May, 2003

TABLE 4 Neurological complications in patients in whom subdural grids were implanted Complication

hemiparesis dysphasia facial weakness visual field defect dysnomia neglect syndrome hemisensorial deficit postop increase in seizures gait disturbance agnosia skew deviation diplopia abducent nerve paralysis third nerve palsy frontal nerve palsy dyslexia–dysgraphia apraxia

Total (%)

24 (69) 18 (51) 17 (48) 13 (37) 12 (34) 10 (28) 7 (20) 5 (14) 5 (14) 2 (6) 2 (6) 2 (6) 2 (6) 2 (6) 2 (6) 2 (6) 2 (6)

Transient (%) Permanent (%)

24 (69) 17 (48) 14 (39) 0 (0) 10 (28) 8 (22) 5 (14) 5 (14) 5 (14) 2 (6) 1 (3) 1 (3) 1 (3) 2 (6) 1 (3) 2 (6) 2 (6)

0 (0) 1 (3) 3 (9) 13 (37) 2 (6) 2 (6) 2 (6) 0 (0) 0 (0) 0 (0) 1 (3) 1 (3) 1 (3) 0 (0) 1 (3) 0 (0) 0 (0)

ported on a patient with a brain tumor who developed signs of increased intracranial pressure caused by cerebral edema after grid implantation, with resultant emergency grid removal and reinsertion 1 week later. In our series, postoperative neuroimaging-verified cerebral edema was encountered in five cases; no patient required an earlier second-stage procedure because of cerebral edema. Only one patient developed moderate acute brain swelling during dural closure after grid implantation. This patient’s bone flap was temporarily removed during the monitoring phase without serious sequelae. To prevent clinically significant cerebral edema from occurring in patients who undergo grid implantation, we have found that the use of large duraplasties and hinging the bone flap at its superior margin with sutures is quite effective. Care must also be taken to ensure that the edges of large grids do not compress and impede the outflow of major draining vessels such as the vein of Labbé or Trolard as they enter the dural venous sinuses. Several patients in our series suffered hemorrhagic adverse events, none of which required an additional surgical session. Five patients had SDHs and four had ICHs. Two patients had epidural fluid collections. Three of the SDHs and two of the ICHs were evacuated at the time of the second craniotomy and grid removal. In six (55%) of the 11 patients in this group the complications were managed conservatively, with no related morbidity observed on followup review, and 45% were treated surgically. In one of the patients with Landau–Kleffner syndrome who underwent extensive MST, an ICH was detected using ultrasonography and evacuated intraoperatively. A second case of ICH diagnosed on CT scans after grid implantation was epileptogenic on EEG, and was thought to be caused by compression of the vein of Labbé by the edges of the grid. This hematoma was evacuated at the second operation with the aid of ultrasonography, and this case illustrates the practical use of intraoperative ultrasonography, especially after extensive MSTs. Once again, avoidance of venous compression by the edges of the grids is emphasized to avoid complications such as ICH.10,29,56 1023

Ç. Önal, et al. Whereas Lee, et al.,29 reported hematomas between the dura mater and subdural grid in some cases, two of our three SDHs were found beneath the grid. Adelson, et al.,2 reported on one case of subacute SDH (3%) in 31 children after subdural grid placement. This patient had undergone previous intracranial surgery and the hematoma was thought to have been caused by subdural scar formation. Behrens, et al.,7 described one patient (7%) who had a clinically silent SDH after grid implantation among 15 such cases; the clot was removed during the second procedure. Kim, et al.,28 reported one hematoma in 27 patients who underwent invasive monitoring. Lee, et al., described four cases of SDH (8%) overlying the grids; these lesions required evacuation, and the electrodes were left in situ for further monitoring. Two cases of transient epileptic foci with intracranial hemorrhage in patients with subdural and epidural electrodes were reported by Wennberg, et al.,62 one of them an SDH overlying the grid and the other a focal intraparenchymal hemorrhage underlying the affected epidural electrodes. Bruce and Bizzi10 emphasized that, to prevent cortical laceration, there should be no sharp edges on the grids if they are cut to a smaller size to fit the targeted region. Because of the large grids that were fashioned in most of our patients, and the large craniotomies that had to be performed as a result, the majority of patients required a blood transfusion at some point during their hospitalization (only 20% of all patients did not require blood transfusion). Blood loss and subsequent transfusions correlated directly and significantly with the size and number of electrodes on the grids. These interesting preliminary observations should be confirmed in larger series. We have found that most of the blood loss in these cases occurs when the large bone flaps are turned at the initial surgery, especially along the most medial parasagittal cuts. Care should be taken in children to strip the dura at the coronal and lambdoid suture lines, because the dura can be quite adherent to the overlying bone in these locations. The large bone flaps should be fashioned quickly, and the medial edges of the craniotomy secured with bone wax and dural tenting sutures to control blood loss. As an alternative to these suggested methods, one could fashion smaller grids routinely, although such smaller grids might not capture critical data regarding the spread of the seizure focus and secondary zones of epileptogenesis. The neurological complications reported here are most likely the result of the extent and location of the cortical resections and/or the MSTs rather than the implantation of the subdural grids or strips. These complications are similar to those reported in the literature for surgery to relieve seizures, such as we have performed.6,20,24,28,37 Seizure outcome in the present series revealed that 80% of patients benefited from surgery, with at least a more than 50% decrease in seizure frequency. Eighty-seven percent of the patients reported on by Adelson, et al.,4 and 80% of the patients by Keene, et al.,25 had outcomes categorized as modified Engel Classes I to III. Using the same scale, Bruce and Bizzi10 reported 73% success in their pediatric extratemporal epilepsy surgery series. Kim, et al.,28 reported 68% good results, with outcomes of Engel Classes I to II in 38 pediatric patients. Favorable results have been reported in pediatric epilepsy surgery series, with the percentage of seizure-free patients ranging from 52 to 78%.4,24,25,28 Fourteen (40%) of 35 patients in our series became seizure free. The relatively low 1024

percentage of such patients in our group may be attributed to the relative absence of patients with tumors, and to the complex nonlesional epilepsy for which invasive monitoring was required.

Conclusions Although serious adverse events related to surgical intervention and chronic invasive monitoring have been noted in this series and in the literature, invasive subdural grid monitoring is a valuable method for localizing the epileptogenic zone and for performing functional mapping in children with epilepsy. Given the acceptable complication rate overall in our series, which spanned 5 years, we believe that carefully selected pediatric patients with intractable epilepsy can be well served by chronic invasive monitoring with subdural grids and/or strips or depth electrodes, and by the planned cortical resections that result from information gathered during this monitoring. It must be acknowledged that the procedures discussed here are significant ones, especially in young children. When possible, complication avoidance strategies for these procedures have been described. Attempts to find accurate, noninvasive strategies to manage seizures in these patients, such as with MEG and new technologies as they evolve, should continue.

References 1. Adelson PD: Temporal lobectomy in children with intractable seizures. Pediatr Neurosurg 34:268–277, 2001 2. Adelson PD, Black PM, Madsen JR, et al: Use of subdural grids and strip electrodes to identify a seizure focus in children. Pediatr Neurosurg 22:174–180, 1995 3. Adelson PD, O’Rourke DK, Albright AL: Chronic invasive monitoring for identifying seizure foci in children. Neurosurg Clin N Am 6:491–504, 1995 4. Adelson PD, Peacock WJ, Chugani HT, et al: Temporal and extended temporal resections for the treatment of intractable seizures in early childhood. Pediatr Neurosurg 18:169–178, 1992 5. Alsaadi TM, Laxer KD, Barbaro NM, et al: False lateralization by subdural electrodes in two patients with temporal lobe epilepsy. Neurology 57:532–534, 2001 6. Behrens E, Schramm J, Zentner J, et al: Surgical and neurological complications in a series of 708 epilepsy surgery procedures. Neurosurgery 41:1–10, 1997 7. Behrens E, Zentner J, van Roost D, et al: Subdural and depth electrodes in the presurgical evaluation of epilepsy. Acta Neurochir 128:84–87, 1994 8. Bhaskara Rao M, Radhakrishnan K, Radhakrishnan VV, et al: Expanding cyst following temporal lobectomy: an unusual complication of epilepsy surgery. Clin Neurol Neurosurg 101:141–144, 1999 9. Breningstall GN: Mortality in pediatric epilepsy. Pediatr Neurol 25:9–16, 2001 10. Bruce DA, Bizzi JWJ: Surgical technique for the insertion of grids and strips for invasive monitoring in children with intractable epilepsy. Childs Nerv Syst 16:724–730, 2000 11. Cascino GD, Sharbrough FW, Trenerry MR, et al: Extratemporal cortical resections and lesionectomies for partial epilepsy: complications of surgical treatment. Epilepsia 35:1085–1090, 1994 12. Chitoku S, Otsubo H, Harada Y, et al: Extraoperative cortical stimulation of motor function in children. Pediatr Neurol 24: 344–350, 2001


Complications of subdural grid monitoring in children 13. Chugani HT: PET in preoperative evaluation of intractable epilepsy. Pediatr Neurol 9:411–413, 1993 14. Cockerell OC, Johnson AL, Sander JW, et al: Mortality from epilepsy: results from a prospective population-based study. Lancet 344:918–921, 1994 15. Donner EJ, Smith CR, Snead OC III: Sudden unexplained death in children with epilepsy. Neurology 57:430–434, 2001 16. Eisenschenk S, Gilmore RL, Cibula JE, et al: Lateralization of temporal lobe foci: depth versus subdural electrodes. Clin Neurophysiol 112:836–844, 2001 17. Elger CE, Burr W: Subdural electrodes. Acta Neurol Scand Suppl 152:44–50, 1994 18. Engel J Jr: Surgery for seizures. N Engl J Med 334:647–652, 1996 19. Goldring S: A method for surgical management of focal epilepsy, especially as it relates to children. J Neurosurg 49:344–356, 1978 20. Hamer HM, Morris HH, Mascha EJ, et al: Complications of invasive video-EEG monitoring with subdural grid electrodes. Neurology 58:97–103, 2002 21. Hodaie M, Musharbash A, Otsubo H, et al: Image-guided frameless stereotactic sectioning of the corpus callosum in children with intractable epilepsy. Pediatr Neurosurg 34:286–294, 2001 22. Irwin K, Birch V, Less J, et al: Multiple subpial transection in Landau-Kleffner syndrome. Dev Med Child Neurol 43:248–252, 2001 23. Jay V, Becker LE, Otsubo H, et al: Pathology of temporal lobectomy for refractory seizures in children. Review of 20 cases including some unique malformative lesions. J Neurosurg 79:53–61, 1993 24. Keene DL, Loy-English I, Ventureyra ECG: Long-term socioeconomic outcome following surgical intervention in the treatment of refractory epilepsy in childhood and adolescence. Childs Nerv Syst 14:362–365, 1998 25. Keene DL, Loy-English I, Ventureyra ECG: Patient satisfaction with surgical treatment of refractory epilepsy done in childhood and early adolescence. Childs Nerv Syst 14:30–32, 1998 26. Keene DL, Ventureyra ECG: The preoperative assessment in the planning of surgical management of medically refractory epilepsy in the pediatric patient. Childs Nerv Syst 16:851–855, 2000 27. Kilpatrick C, Cook M, Kaye A, et al: Non-invasive investigations successfully select patients for temporal lobe surgery. J Neurol Neurosurg Psychiatry 63:327–333, 1997 28. Kim SK, Wang KC, Hwang YS, et al: Pediatric intractable epilepsy: the role of presurgical evaluation and seizure outcome. Childs Nerv Syst 16:278–286, 2000 29. Lee WS, Lee JK, Lee SA, et al: Complications and results of subdural grid electrode implantation in epilepsy surgery. Surg Neurol 54:346–351, 2000 30. Leinonen E, Tuunainen A, Lepola U, et al: Postoperative psychoses in epileptic patients after temporal lobectomy. Acta Neurol Scand 90:394–399, 1994 31. Leiphart JW, Peacock WJ, Mathern GW: Lobar and multilobar resections for medically intractable pediatric epilepsy. Pediatr Neurosurg 34:311–318, 2001 32. Lhatoo SD, Johnson AL, Goodridge DM, et al: Mortality in epilepsy in the first 11 to 14 years after diagnosis: multivariate analysis of a long-term, prospective, population-based cohort. Ann Neurol 49:336–344, 2001 33. Malow BA, Sato S, Kufta CV, et al: Hematoma-related seizures detected during subdural electrode monitoring. Epilepsia 36: 733–735, 1995 34. Manji H, Plant GT: Epilepsy surgery, visual fields, and driving: a study of the visual field criteria for driving in patients after temporal lobe epilepsy surgery with a comparison of Goldmann and Esterman perimetry. J Neurol Neurosurg Psychiatry 68:80–82, 2000 35. McLachlan RS: Commentary on epilepsy surgery in Canada. Can J Neurol Sci 28:4–5, 2001


36. Minassian BA, Otsubo H, Weiss S, et al: Magnetoencephalographic localization in pediatric epilepsy surgery: comparison with invasive intracranial electroencephalography. Ann Neurol 46:627–633, 1999 37. Morrison G, Duchowny M, Resnick T, et al: Epilepsy surgery in childhood. A report of 79 patients. Pediatr Neurosurg 18: 291–297, 1992 38. Nordli DR Jr, Kelley KR: Selection and evaluation of children for epilepsy surgery. Pediatr Neurosurg 34:1–12, 2001 39. Olson DM: Evaluation of children for epilepsy surgery. Pediatr Neurosurg 34:159–165, 2001 40. Otsubo H, Chuang SH, Hwang PA, et al: Neuroimaging for investigation of seizures in children. Pediatr Neurosurg 18:105–116, 1992 41. Otsubo H, Hwang PA, Jay V, et al: Focal cortical dysplasia in children with localization-related epilepsy: EEG, MRI, and SPECT findings. Pediatr Neurol 9:101–107, 1993 42. Otsubo H, Shirasawa A, Chitoku S, et al: Computerized brain surface voltage topographic mapping for localization of intracranial spikes from electrocorticography. Technical note. J Neurosurg 94:1005–1009, 2001 43. Otsubo H, Snead OC III: Magnetoencephalography and magnetic source imaging in children. J Child Neurol 16:227–235, 2001 44. Otsubo H, Steinlin M, Hwang PA, et al: Positive epileptiform discharges in children with neuronal migration disorders. Pediatr Neurol 16:23–31, 1997 45. Ozkara C, Ozyurt E, Hanoglu L, et al: Surgical outcome of epilepsy patients evaluated with a noninvasive protocol. Epilepsia 41 (Suppl 4):S41–S44, 2000 46. Pomata HB, Gonzales R, Bartuluchi M, et al: Extratemporal epilepsy in children: candidate selection and surgical treatment. Childs Nerv Syst 16:842–850, 2000 47. Rosen I: Subdural electrodes: discussion. Acta Neurol Scand Suppl 152:53–55, 1994 48. Rosenbaum TJ, Laxer KD, Vessely M, et al: Subdural electrodes for seizure focus localization. Neurosurgery 19:73–81, 1986 49. 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 39:327–334, 1996 50. Rutka JT, Otsubo H, Kitano S, et al: Utility of digital camera-derived intraoperative images in the planning of epilepsy surgery for children. Neurosurgery 45:1186–1191, 1999 51. Siegel AM, Roberts DW, Thadani VM, et al: The role of intracranial electrode reevaluation in epilepsy patients after failed initial invasive monitoring. Epilepsia 41:571–580, 2000 52. Snead OC III, Nelson MD Jr: PET does not eliminate need for extraoperative, intracranial monitoring in pediatric epilepsy surgery. Pediatr Neurol 9:409–411, 1993 53. Spencer SS, Spencer DD, Williamson PD, et al: Combined depth and subdural electrode investigation in uncontrolled epilepsy. Neurology 40:74–79, 1990 54. Sperling MR, O’Connor MJ: Comparison of depth and subdural electrodes in recording temporal lobe seizures. Neurology 39: 1497–1504, 1989 55. Stapleton SR, Kiriakopoulos E, Mikulis D, et al: Combined utility of functional MRI, cortical mapping, and frameless stereotaxy in the resection of lesions in eloquent areas of brain in children. Pediatr Neurosurg 26:68–82, 1997 56. Swartz BE, Rich JR, Dwan PS et al: The safety and efficacy of chronically implanted subdural electrodes: a prospective study. Surg Neurol 46:87–93, 1996 57. Thadani VM, Williamson PD, Berger R, et al: Successful epilepsy surgery without intracranial EEG recording: criteria for patient selection. Epilepsia 36:7–15, 1995 58. Uematsu S, Lesser R, Fisher R, et al: Resection of the epileptogenic area in critical cortex with the aid of a subdural electrode grid. Stereotact Funct Neurosurg 54/55:34–45, 1990 59. Van Ness PC, Morris HH III: Transient localized periodic epilepti-

1025

Ç. Önal, et al.

60. 61. 62.

63. 64. 65.

form discharges detected by intracerebral depth electrodes after intracerebral hematoma. Neurology 44 (Suppl 2):A233–A234, 1994 (Abstract) Van Veelen CWM: Subdural and intracerebral recording in presurgical evaluation of epilepsy. Acta Neurol Scand Suppl 152: 51–52, 1994 Van Veelen CWM, Debets RMC, van Huffelen AC, et al: Combined use of subdural and intracerebral electrodes in preoperative evaluation of epilepsy. Neurosurgery 26:93–101, 1990 Wennberg R, Gross D, Quesney F, et al: Transient epileptic foci associated with intracranial hemorrhage in patients with subdural and epidural electrode placement. Clin Neurophysiol 110: 419–423, 1999 Wyler AR, Hermann BP, Richey ET: Results of reoperation for failed epilepsy surgery. J Neurosurg 71:815–819, 1989 Wyler AR, Ojemann GA, Lettich E, et al: Subdural strip electrodes for localizing epileptogenic foci. J Neurosurg 60:1195–1200, 1984 Wyler AR, Walker G, Somes G: The morbidity of long-term sei-

1026

zure monitoring using subdural strip electrodes. J Neurosurg 74: 734–737, 1991 66. Wyllie E, Luders H, Morris HH III, et al: Clinical outcome after complete or partial cortical resection for intractable epilepsy. Neurology 37:1634–1641, 1987 67. Zentner J, Hufnagel A, Ostertun B, et al: Surgical treatment of extratemporal epilepsy: clinical, radiological, and histopathologic findings in 60 patients. Epilepsia 37:1072–1080, 1996 68. Zumsteg D, Wieser HG: Presurgical evaluation: current role of invasive EEG. Epilepsia 41 (Suppl 3):S55–S60, 2000

Manuscript received April 30, 2002. Accepted in final form February 10, 2003. Address reprint requests to: James T. Rutka, M.D., Ph.D., Division of Neurosurgery, Suite 1504, The Hospital for Sick Children, 555 University Avenue, Toronto, Ontario, Canada M5G 1X8. email: [email protected].
