Surgery is an accepted tool to treat medically refractory epilepsy.1 In contrast to epilepsy associated with single lesions or mesial temporal sclerosis, nonlesional epilepsy or epilepsy associated with multiple lesions necessitates accurate preresection mapping of the epileptogenic zone (EZ).2 This is especially important in multifocal epilepsies, in particular, those associated with malformations of cortical development, as seen in tuberous sclerosis complex (TSC). After noninvasive studies (such as surface video EEG [VEEG], magnetoencephalography [MEG], and positron emission tomography [PET], and single-photon emission computer tomography [SPECT]), the EZ often remains poorly defined. Several invasive techniques have been used to better define the EZ, including stereo EEG,3 subdural strips and grids,4 and depth electrodes.5
In previous publications, we described our surgical technique and rationale for performing staged surgical procedures for TSC-related refractory epilepsy.6 This approach involves at least 2 surgeries, including an invasive recording phase followed by resection of epileptic tissue. This approach has resulted in improvements in both the patient’s and the family's quality of life and, not infrequently, seizure freedom with a low complication rate.7
Despite our previous publications describing the efficacy of staged epilepsy surgery on the epileptic disease, including in refractory multifocal epilepsy (such as TSC), this approach is not widely practiced.6 The reasons for reluctance to apply such a surgical strategy may be related to concerns over potential complications that may arise from multiple surgical procedures.
This study involves a retrospective chart review to evaluate the safety of staged surgical treatments for refractory epilepsy among children. In this article, epilepsy outcomes are not reported.
PATIENTS AND METHODS
Study Design and Setting
This was a retrospective study. Over 12.5 years (September 1996 through March 2009), 161 children (younger than 18 years of age) underwent intracranial monitoring for the treatment of epilepsy. The decision regarding such a surgical approach is made after a thorough preoperative evaluation at the Comprehensive Epilepsy Center (CEC) at the NYU Langone Medical Center. This includes a thorough neurological and neuropsychological evaluation, prolonged scalp VEEG monitoring, and various complementary tests such as PET, SPECT, and MEG. All cases are discussed at the weekly multidisciplinary presurgical conference together with the epileptology, neuropsychology, neuroradiology, and surgical teams; a consensus recommendation is formulated for each patient. For the sake of clarity, the term admission relates to a multistage procedure.
All children (younger than 18 years of age) who underwent invasive intracranial monitoring for epilepsy treatment were included in this study.
A typical admission with a staged procedure consists of at least 2 surgeries. During the first, a set of invasive electrodes (consisting of subdural strips, grids, and often depth electrodes) is placed either unilaterally or bilaterally. In some patients with well-defined, potentially epileptogenic lesions, a focal resection of the lesion is performed in the first surgical stage before electrode implantation. After implantation of electrodes, all children are monitored in the pediatric intensive care unit. The duration of invasive VEEG monitoring is primarily determined by the data captured; the epileptologists determine when adequate interictal and ictal data have been captured. Bedside cortical stimulation for functional mapping is performed in cases in which the surgical plan necessitates further delineation of the epileptogenic zone vs function/eloquent cortices, especially in older children.8 Throughout monitoring, patients are monitored for signs of central nervous system (CNS) infection; if such signs are present, VEEG monitoring may be shortened. At the second-stage surgery, the intracranial electrodes are removed, and, when possible, a suitable resection of the EZ is performed. For a subset of patients, additional intracranial electrodes may be implanted to verify complete removal of the focus and/or identify additional adjacent or distant foci that may remain or become apparent after removal of the previous one.9,10 The third stage is performed in a similar fashion; the electrodes are usually not reimplanted at the third stage. However, in very rare cases in this cohort, they were reimplanted leading to a fourth surgical stage.
To reduce complications, we adopted a series of standard practices:
1. A 7-mm Jackson-Pratt subgaleal drain is left in place as long as there are electrodes and for 2 to 3 days after the final stage. The drain is removed and replaced at each operation.
2. A mini-craniotomy is performed for the insertion of only strips to achieve a comfortable exposure and to better control the strip insertion.
3. The electrodes are fixed to the dura with sutures to prevent migration.
4. The dura is closed in a loose fashion, in as much as possible a water tight manner, using an autologous periosteal graft, which is harvested from the craniotomy flap. This is done to minimize cerebrospinal fluid (CSF) leaks and to prevent elevated intracranial pressure from the electrodes.
5. The electrode wires are tunneled subcutaneously and through small puncture holes (using a trocar). Each wire is secured with a 4-0 nylon purse-string suture to prevent a CSF leak as much as possible. All electrodes are tied together and to the skin using a 0-Prolene suture to prevent inadvertent pulling.
6. The bone flap is washed with saline solution and antibiotics before placement. Titanium miniplates are attached to the free bone flap; however, only 1 is also secured to the cranium. This enables the bone to hinge outward and avoids compression of the brain in cases in which the subdural electrodes cause mass effect. At the final stage, the bone is firmly fixed using the titanium plates.
7. After removal of electrodes and drains, the wire exit holes in the skin are obliterated using a 4-0 Monocryl suture to prevent a CSF fistula.
a. Steroids: All patients receive dexamethasone (4-6 mg) during surgery, followed by 8 to 16 mg daily that is tapered over approximately 1 week.
b. Antibiotics: Perioperatively, patients receive 1 dose of cefazolin (if not allergic), to be followed by a daily dose of cefazolin until the second-stage surgery. At the second and third surgeries, vancomycin and either cefipime or ceftriaxone are given perioperatively. At each surgical stage (starting with the second), screening epidural and subdural swab cultures are taken during surgery. Vancomycin and cefipime or ceftriaxone are continued for 3 days (until final culture results are negative), then switched back to cefazolin until the following stage or until all drains are removed. If a screening culture returns positive results, relevant antibiotics are given for an additional period of time as clinically indicated, and electrodes are removed. We believe that this may aid in early infection detection, although there is no clear support that this routine will change infectious care.
Data Collection and Variables
After obtaining institutional review board approval, the data were retrospectively collected. Patient names were taken from the epilepsy surgery registry at our unit. The patients' demographic factors, clinical history, and indications for surgery were collected from the office charts and the CEC preoperative conference summary. Operative details including the type and number of electrodes placed were gathered from the operative notes. The immediate postoperative course was taken from the office charts and the discharge letters. Long-term follow-up, including late complications, were taken from the office charts. For the purpose of this study, we defined permanent neurological deficits as unexpected new (or exacerbated) neurological deficits (as opposed to hemiparesis after hemispherotomies or rolandic region operations, and visual field disturbances after posterior region operations).
Major complications included death, new permanent neurological deficits (which were unexpected before surgery), the need for any immediate surgery (<2 weeks after the primary surgery), and active CNS infection (such as brain abscess and meningitis). Minor complications included a positive screening sub-/epidural culture in an asymptomatic patient, noninfectious fevers, and bone absorption.
Data were entered in an Excel worksheet and analyzed using the SPSS software (SSPS Inc, version 16.0.2, Chicago, Illinois). Specifically, patients were determined to have either focal or multifocal epilepsy and the etiologies (and frequencies thereof) were recorded and calculated. Next, the total number of surgeries was recorded for each visit. It was also recorded whether patients had unilateral or bilateral monitoring and the surgical approach taken, where relevant. The duration of monitoring was also determined (total number of days), as was total length of hospitalization (total days). Time to follow-up was also recorded. Next, surgical complications were recorded (types and totals). Data were expressed as percentages of patients, admissions, and surgeries.
Correlation analyses assessed the relationship between relevant variables such as age at surgery, number of surgeries, number of admissions, total number of surgeries, number of sides operated on, duration of monitoring, and length of hospitalization. χ2 analyses assessed for differences in the complication rates between the first 100 surgeries and the second 100 surgeries, the first 6 years of surgeries and the next 6 years, and those undergoing intracranial monitoring and those undergoing monitoring with subsequent resection.
Over 12.5 years (September 1996 through March 2009), 161 patients underwent staged epilepsy surgeries. Age at surgery ranged from 8 months to 16.5 years (mean, 7.1 ± 4.2 years). Epilepsy was focal in 25 children and multifocal in 136. Multifocal epilepsy was defined based on multiple locations of seizure onset zones as seen on VEEG. Etiologies are summarized in Table 1.
A total of 200 admissions for staged procedures were performed, with a span of 1 to 4 admissions per patient (1.2 ± 0.5). The total number of surgeries was 496, with a span of 2 to 10 per patient (3 ± 1.5), and 2 to 4 (2.5 ± 0.6) surgeries per admission. Fifteen children had previous intracranial surgeries elsewhere. Table 2 summarizes the number of surgeries in each admission.
Of the 200 admissions, 139 (69.5%) were unilateral invasive monitoring, and 61 (30.5) were bilateral. Forty-one admissions (20%) included invasive monitoring with no resections, and 159 (80%) included resection and invasive monitoring. Of the 496 surgeries, 250 included resection and electrode placement, 189 involved electrode placement only, and the remaining 57 surgeries were electrode removal only. Total duration of invasive monitoring (from insertion to final removal) was 1 to 30 days (10 ± 4 days). Length of hospitalization was 6 to 38 days (16 ± 5 days).
Time from last admission to last follow-up or between admissions ranged from 1 to 120 months (21 ± 26 months).
Outcome Data and Main Results
Table 3 summarizes the complication rates per surgery, admission, and patient. The 3 most common complications included positive screening cultures (subdural or epidural) in asymptomatic patients, noninfectious fevers, bone absorption, wound complications, and hydrocephalus, composing all together, more than 50% of the total complications. Permanent neurological complications included 4 cases of new (or exacerbated) hemiparesis.
Complications Necessitating Surgical Treatment
Twenty-five patients underwent 30 surgeries treating various complications. Six surgeries in 6 patients occurred within 2 weeks (risk of 1.2% per surgery, 3% per admission, and 3.7% per patient), whereas 24 surgeries in 19 patients occurred after 2 weeks (risk of 4.8% per surgery, 12% per admission, and 14.9% per patient). Table 4 summarizes the surgical complications, and Table 5 displays the layout of surgical complications in relation to number of surgeries and admissions.
Risk Factors for Complication
There were no significant correlations between complication rates and the number of surgeries per admission or the number of admissions. However, the complication rate was significantly lower among the last 100 admissions relative to the first 100 (16% vs 23%, P = .05) and during the last 6 years relative to the first 6 years (15% vs 30%, P < .0001). Table 6 summarizes the complication rate comparison according to various parameters. Although not significant, there was a trend for patients undergoing resections having more complications than those undergoing only intracranial EEG (P = .09). Spearman correlation coefficients showed that the complication risk was correlated with younger age at the time of surgery and longer hospitalization (Table 7), whereas other factors were not significant predictors of complication risk; the rate of complication was not correlated with number of admissions, total number of surgeries, number of sides operated on, or total duration of monitoring. Specifically, the number of surgeries per admission (2 or >2) did not have an effect on the rate of complications (Tables 6 and 7).
We present the largest series of children undergoing staged procedures with invasive EEG monitoring with a long-term follow-up. Most patients had multifocal epilepsy due to TSC or unknown causes. Of 161 children, 32 underwent more than 1 staged procedure (ie, >1 admission for surgery) because of seizure recurrence after the first surgery. Thus, most children underwent only 1 admission, most of which included 2 or 3 surgeries.
The general complication rates were not significantly different between the various subgroups and were not affected by the number of surgeries that the patients underwent or by the number of admissions (ie, if it was the first, second, or third admission). Specifically, the unique group of patients who underwent 3 and 4 surgeries during 1 admission had complication rates similar to those who underwent only 2 surgeries during an admission. Notably, surgical experience appeared to lower the complication rate, as demonstrated by the difference between the first and last 100 admissions and the difference between the first and second half of the surgical epoch. We could not find a clear explanation for this difference, as we did not make any major changes in the surgical technique over time; however, we assume that with experience, additional care was applied to small details such as wire fixations, dura closure with a periosteal graft, wound care, and bone fixation, as well as other patient care and routines (as described in the Methods section), which were adapted and refined. Another explanation for the lower complication rate between remote and recent periods may be differences in patient populations. Also, as expected, complications were more frequent in patients undergoing resection(s) as opposed to those in whom only intracranial EEG was performed. In these analyses, younger age was significantly associated with a slight increase in complication rate. This said, the actual magnitude of the correlation was quite small (r = 0.194, small effect size), and the statistical significance reflects the large sample size rather than a large effect; age accounted for less than 4% of the variance in complication rate (r2 = 0.038). As such, the added risk is considered limited. Prolonged hospitalization was also significantly associated with an increased complication rate, although, again, the actual magnitude of the correlation was small and length of hospitalization accounts for only about 2% of the variance in complication rate (r2 = 0.02). The duration of intracranial EEG monitoring and the number of stages and surgeries were not associated with complications. Although a strict causal relationship cannot be determined, the lack of significance of surgical stages and duration of monitoring suggests that the increased hospital stay is related to the complication; if the prolonged stay caused the complication, one would expect that duration of monitoring would be associated with complications as well.
Surgical resection of epileptic foci is a well-accepted treatment for refractory epilepsy, with seizure control rates in the range of 50% to 90% depending on multiple factors, including pathology, location, duration of seizures, and extent of resection.5,6,11-22 In contrast to single lesional epilepsy and mesial temporal sclerosis, some focal epileptic disorders have no clearly defined seizure focus based on magnetic resonance imaging and VEEG studies. Such challenges may result from diffuse or multifocal interictal and ictal foci. Such patients are often excluded as epilepsy surgery candidates. A classic example of this anatomoelectrical complexity is tuberous sclerosis.6 These children often have multifocal or symptomatic generalized epilepsy, with multiple tubers and multifocal epileptic foci on VEEG, PET, SPECT, and MEG. Thus, these children are often not considered as candidates for resective surgery.
Over the past 15 years, our center has adopted a surgical approach combining invasive EEG monitoring, when indicated, with seizure focus resection. Our seizure and quality of life outcomes in children with TSC-related epilepsy, for example, have shown that 70% of children have at least a 90% reduction of seizures, coupled with improved patient and family quality of life.6,7 We use similar surgical techniques for other challenging cases besides TSC, including malformations of cortical development. The decision to proceed with a staged approach rather than a simple single-stage resection for a specific patient is made collectively at our CEC conference with epileptologists and neurosurgeons.
Applying a staged approach with multiple potential surgeries would theoretically pose a risk to the patient as well as a burden on the family and child. Nevertheless, when considering the risk-benefit profile in these children with severe epileptic disorders, we found that the benefits outweigh the risks. We systematically surveyed the families of children with TSC who underwent epilepsy surgery. Despite a prolonged hospital course with a least 2 operations, 37 of 39 families were extremely satisfied and would have undergone the entire procedure again if they had known all that actually happened, including complications and length of stay.7 In a previous study of staged epilepsy surgery by our group, two thirds had a new neurological deficit; however, 80% were transient. In that series, we stated 20% non–CNS-related infections, 15% noninfectious fevers, and 15% hydrocephalus.9 However, 60% of children had an Engel class I outcome. Similarly high epilepsy control rates were achieved using staged resections for treating tuberous sclerosis–related epilepsy in children.6 Thus, the advantage of epileptic control may justify potential risks, especially in severely refractory seizures, where the risk of the natural history, including sudden death, may be significant. In this study, we focused only on the complications of this approach.
Interpretation and Generalizability
Comparing the results of the current series with previously published series of epilepsy surgery complications is not straightforward. The epilepsy surgery literature has focused on complications of pure resective procedures such as temporal lobectomies, hemispherotomies, tumor resections, and other epileptic foci resections.23 Here, we focused exclusively on invasive monitoring–related complications with a minority of patients having undergone only invasive monitoring without a subsequent resection.
Additionally, the definition of a complication is neither precise nor uniform in the literature.24 Neurological complications are more common, yet often anticipated, after epilepsy surgery. These include visual field defects after temporal and occipital lobectomies and sensorimotor compromises after rolandic resections.15,24,25 Noninfectious postoperative fever and the need for future shunts are common findings after hemispherotomies and hemispherectomies.11,23,25-27
Some complications may be underdiagnosed, such as postoperative subdural collections and brain contusions after invasive monitoring, which appear in about 25% to 35% of patients, but are often asymptomatic.28 We did not include asymptomatic postoperative hemorrhages as complications in this series because they had no clinical significance and did not alter the treatment in any way. Further, the rate of asymptomatic complications such as bleeds is likely a function of the vigilance by which it is assessed and the sensitivity of the measure.
Although there are several series with relatively large patient volumes, comparisons between centers and series in the existing literature are often challenging due to the variations in both surgical techniques and the definitions of complications. Examples for this surgical technique diversity are the inclusions of subgaleal drains, removal of the bone flap (and reimplantation at the final surgical stage), use of osteoplastic flaps or artificial dural substitutes, and the use of perioperative steroids. To date, the largest review regarding complications of epilepsy surgery was published in 2013 by Hader et al.29 They reviewed the English literature from 1990 until 2008 and included all relevant series with at least 20 patients. They excluded hypothalamic hamartoma cases, disconnection procedures (hemispherotomies and callosotomies), and multiple subpial transections. Also excluded were series focusing on lesion resections (such as tumors, cavernomas, and arteriovenous malformations). Eventually they included 76 papers in their review, including about 4800 patients (of all ages). Overall, the rate of minor medical complications (such as CSF leaks, CNS infections or bleeds, metabolic abnormalities, and thromboembolic complications) was 7.7% for invasive monitoring and 5.1% for resections. The most common complication was CSF leak (∼8.5%), followed by aseptic meningitis (3.6%), bacterial intracranial infection (3%), and intracranial hematoma (2.5%). All complications were significantly more common in children than in adults. In another recent meta-analysis from 2013, Arya et al30 reviewed the complications of invasive monitoring using subdural grids. Reviewing 21 publications since 1984 and including 2542 patients of all ages, the authors calculated the pooled risks and found the following: the risk of CNS bacterial infection, 2.3%; bone flap infection, 1.8%; wound infection, 3%; positive culture in asymptomatic patients, 7%; intracranial bleed, 4% (a third necessitating surgery); CSF leak, 12%; increased intracranial pressure, 2.4%; and transient neurological complications, 4.6%. Altogether, 3% of patients underwent an additional surgery for treatment of any complication. Despite these pooled rates, various studies regarding the use of subdural grids or strips have stated higher complication rates, including neurological complications up to 15%, 15% infection rate, 20% to 30% CSF leak rate, 25% hemorrhage rate (most with no clinical importance), 40% noninfectious fever rate, and a total complication rate up to approximately 40%; however, among the different series, rates vary significantly and often include minor and major complications.21,22,31-37 Postoperative fevers with negative cultures, as well as positive screening cultures in asymptomatic patients, are common after invasive monitoring and occur in up to 20% of patients.33,34 Some contributing factors reported to be associated with an increased risk of CNS infection are the number of electrodes, the number of tunneled wires, and the duration of monitoring30,37; however, these risk factors are not found by all groups.4,38 Additionally, subdural grids may cause cerebral edema leading to routine use of perioperative steroids by many groups.31,39,40 Another study of pediatric epilepsy outcome over 22 years (425 children) found a total complication rate of 9.2%; however, they did not include the need for a shunt as a complication (occurring in 20% of the entire group and in 40% after hemispherectomies).11 Thus, our rates of CSF leaks, hemorrhages, infections, and need for additional surgery (treating any complication) seem well within the quoted rates in the literature on epilepsy surgery (especially when involving invasive monitoring). Similar to Heller et al, 41 our complication rate decreased with time, possibly reflecting more experience and commitment to meticulous technique.
Some of the complications included in the current series were relatively mild, such as a positive screening sub-/epidural culture in an asymptomatic patient. Similarly, noninfectious fevers and bone absorption are minor complications. We define major complications as death, new neurological deficit (unexpected), the need for immediate surgery, and active CNS infection (such as brain abscess and meningitis). Thus, focusing on this definition of “major” complications, we had no surgery-related mortality; the CNS infection rate was 0.6% per surgery (1.5% per admission), new and unexpected neurological deficit rate was 0.8% per surgery (2% per admission), and the need for an immediate surgery rate was 1.2% per surgery (3% per admission). Thus, overall, despite multiple surgeries combining invasive monitoring and resections, the actual complication rates are comparable to those published for nonstaged epilepsy surgery.
This study has several limitations. Retrospective data collection, heterogeneous population (relating to epileptic etiology and surgical procedures), small group numbers (eg, patients undergoing >2 admissions), and limited follow-up for some patients are important limitations. However, we believe that the large number of consecutive patients undergoing 1 or 2 admissions and the large number of procedures provides a unique addition to the literature on the safety of epilepsy surgery in children. We believe that major complications (such as CNS infections, new unexpected neurological deficits, and conditions leading to early surgical treatment such as hematomas) most often were diagnosed during the postoperative period and were not missed. Other, more minor complications (such as bone absorption) may be underdiagnosed. Moreover, the inclusion of this heterogeneous range of patients reflects that seen in a large academic epilepsy center and thus should have broad practical implications for many centers.
Another major limitation is that for comparison purposes, we combined complications such as infections and hemorrhages. However, as the breakdown of complications was small, and any single complication may affect the statistical results; in addition to presenting the absolute numbers of each complication, we performed a general complication burden comparison between groups and show that the differences are small.
Despite these limitations, the major morbidity rates, such as infections and hematomas, were low, comparable to elective neurosurgery-related morbidity, and we had no mortality.
Staged epilepsy surgery, with invasive electrode monitoring, is relatively safe in children with poorly localized medically refractory epilepsy. The rate of major complications is low and appears comparable to that associated with other elective neurosurgical procedures. Another important conclusion is that with experience, our complication rate decreased.
The authors have no personal or institutional financial interest in drugs, materials, or devices described in this paper.
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The authors describe a unique approach to pediatric epilepsy surgery that they have developed and refined over a long period. Their approach involves the frequent use of multistage surgery. Approximately 45% of the admissions described in this paper included 3- or 4-stage surgical procedures, and 20% included bilateral intracranial EEG placement for localization of seizure onset. This approach offers the hope of seizure control in a group of children with difficult-to-localize seizure onset, many of them with tuberous sclerosis. This paper details the complications associated with this approach in 200 admissions spanning a 12-year period.
Although the data were collected retrospectively, an extensive range of complications are included in this work. The authors report no mortality and only a 2% rate of unexpected neurological morbidity. These numbers compare favorably with 2-stage epilepsy surgeries (by far more common than the multistage procedures described) and with elective intracranial procedures more broadly. Wound complications including infections and bone absorption occurred in 9.5% of patient admissions, a rate slightly higher than identified in a recent meta-analysis of staged pediatric epilepsy surgeries (almost exclusively 2-stage surgeries). The rate of complications requiring surgical intervention was 15%, also higher than in the recent meta-analysis.1 These findings are perhaps not surprising given the complexity of this patient group and the extent of the surgeries performed. It is notable, however, that in the current series, the authors found no correlation between the number of surgical stages and complications.
These data provide valuable context to practitioners and patients weighing the decision of multistage epilepsy surgery.
1. Arya R, Mangano FT, horn PS, Holland KD, Rose DF, Glauser TA. Adverse events related to extraoperative invasive EEG monitoring with subdural grid electrodes: a systematic review and meta-analysis. Epilepsia. 2013;54(5):828–839. View Full Text | PubMed | CrossRef Cited Here... |