A meta-analysis of predictors of seizure freedom in the surgical management of focal cortical dysplasia

Clinical article

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Object

Focal cortical dysplasia (FCD) is one of the most common causes of medically refractory epilepsy leading to surgery. However, seizure control outcomes reported in isolated surgical series are highly variable. As a result, it is not clear which variables are most crucial in predicting seizure freedom following surgery for FCD. The authors' aim was to determine the prognostic factors for seizure control in FCD by performing a meta-analysis of the published literature.

Methods

A MEDLINE search of the published literature yielded 37 studies that met inclusion and exclusion criteria. Seven potential prognostic variables were determined from these studies and were dichotomized for analysis. For each variable, individual studies were weighted by inverse variance and combined to generate an odds ratio favoring seizure freedom. The methods complied with a standardized meta-analysis reporting protocol.

Results

Two thousand fourteen patients were included in the analysis. The overall rate of seizure freedom (Engel Class I) among patients undergoing surgery for FCD in the cohort of studies was 55.8% ± 16.2%. Partial seizures, a temporal location, detection with MRI, and a Type II Palmini histological classification were associated with higher rates of postoperative seizure control. As a treatment-related factor, complete resection of the anatomical or electrographic abnormality was the most important predictor overall of seizure freedom. Neither age nor electroencephalographic localization of the ictal onset significantly affected seizure freedom after surgery.

Conclusions

Using a large population cohort pooled from the published literature, an analysis identified important factors that are prognostic in patients with epilepsy due to FCD. The most important of these factors—diagnostic imaging and resection—provide modalities through which improvements in the impact of FCD can be effected.

Abbreviations used in this paper:EEG = electroencephalography; FCD = focal cortical dysplasia.

Abstract

Object

Focal cortical dysplasia (FCD) is one of the most common causes of medically refractory epilepsy leading to surgery. However, seizure control outcomes reported in isolated surgical series are highly variable. As a result, it is not clear which variables are most crucial in predicting seizure freedom following surgery for FCD. The authors' aim was to determine the prognostic factors for seizure control in FCD by performing a meta-analysis of the published literature.

Methods

A MEDLINE search of the published literature yielded 37 studies that met inclusion and exclusion criteria. Seven potential prognostic variables were determined from these studies and were dichotomized for analysis. For each variable, individual studies were weighted by inverse variance and combined to generate an odds ratio favoring seizure freedom. The methods complied with a standardized meta-analysis reporting protocol.

Results

Two thousand fourteen patients were included in the analysis. The overall rate of seizure freedom (Engel Class I) among patients undergoing surgery for FCD in the cohort of studies was 55.8% ± 16.2%. Partial seizures, a temporal location, detection with MRI, and a Type II Palmini histological classification were associated with higher rates of postoperative seizure control. As a treatment-related factor, complete resection of the anatomical or electrographic abnormality was the most important predictor overall of seizure freedom. Neither age nor electroencephalographic localization of the ictal onset significantly affected seizure freedom after surgery.

Conclusions

Using a large population cohort pooled from the published literature, an analysis identified important factors that are prognostic in patients with epilepsy due to FCD. The most important of these factors—diagnostic imaging and resection—provide modalities through which improvements in the impact of FCD can be effected.

Focal cortical dysplasia is a common cause of intractable epilepsy in both adults and children.43 However, seizure control rates reported in single-institution surgical series range from 8% to 80%. Given these variable results, it is therefore not clear what factors predict a favorable prognosis following surgery for FCD (Table 1).

TABLE 1:

Population characteristics and outcomes of epilepsy surgery for FCD by study*

Authors & YearNo. of PatientsMean Age at Surgery (yrs)% w/ Engel I OutcomePredictors of Favorable Outcome
Alexandre et al., 200641NR63.4temporal location, regional localization of ictal onset
Chang et al., 201114321.070.0complete resection, Barkovich Class I
Chapman et al., 200524NR37.0
Chassoux et al., 200028NR64.0complete resection
Choi et al., 200415024.339.3increased cortical disorganization
Cohen-Gadol et al., 20042226.072.7complete resection
Cossu et al., 20081138.861.0complete resection, temporal location, single MRI-defined lesion, older age at seizure onset
Edwards et al., 20003514.049.0
Fauser et al., 20046721.366.0mild pathological features (mMCD & FCD Type I)
Fountas et al., 20041321.846.2age <18 yrs, normal MRI
Francione et al., 2003106.070.0
Gupta et al., 2004158.066.7
Hader et al., 2004399.654.0complete resection
Hamiwka et al., 2005389.640.0complete resection
Hirabayashi et al., 19931715.535.3temporal or frontal location, single EEG focus
Hong et al., 20003621.355.6complete resection
Hudgins et al., 2005157.866.7MRI-defined lesion, increased cortical disorganization
Keene et al., 199870NR54.0
Kim et al., 20043825.039.5
Kim et al., 200916624.756.6complete resection, partial seizures, severe pathological features (FCD Type II)
Kral et al., 20035324.072.0
Krsek et al., 200936149NR55.0complete resection
Krsek et al., 20093840NRNRsevere pathological features (FCD Type II)
Lerner et al., 200997NRNR
Lortie et al., 200228NR53.3
Palmini et al., 19914824NR8.3complete resection
Palmini et al., 199534NRNRcomplete resection
Park et al., 20063010.367.0temporal location
Phi et al., 2010419.046.0complete resection, MRI-defined lesion
Sarkis et al., 20103914.8NRcomplete resection
Siegel et al., 20062132.752.0shorter duration of epilepsy
Tassi et al., 20011324.076.9severe pathological features (FCD Type II)
Tassi et al., 20025218.064.9
Taylor et al., 19711027.160.0complete resection
Urbach et al., 200222NR86.4
Widdess-Walsh et al., 2005145NR63.0severe pathological features (FCD Type II), lack of need for invasive monitoring
Wyllie et al., 1998136NRNRtemporal location

* mMCD = mild malformation of cortical development; NR = not reported.

Since its original description by Taylor et al.,57 FCD has come to be appreciated as a spectrum of disease rather than a single entity. Mild forms of FCD are difficult to recognize routinely on MRI and often are excluded from clinical analyses and nomenclature systems.2,5 As a result, controversy exists regarding the utility of neuroimaging in predicting seizure-free outcomes following surgery for FCD (Table 1).15,21,30,52 Moreover, the lack of agreement on which FCD subtype (FCD Type I or FCD Type II) best predicts seizure freedom has not been completely resolved.8,20,33,38,56,60 Nevertheless, prior outcome studies have reported specific demographic and perioperative factors that may be important in understanding the prediction of seizure freedom following surgery for FCD. Recent systematic analyses have attempted to pool several of these studies together to test hypotheses regarding predictors of surgical outcome in FCD cases; however, no meta-analysis of predictors determining seizure freedom after surgery for FCD has been performed.11,39 We used meta-analytical techniques to specifically address these issues while statistically minimizing interstudy heterogeneity and population size differences. In this study, we applied these methods to 37 surgical studies in the FCD literature to reach conclusions regarding variables important for a seizure-free outcome following surgical management of this disorder.

Methods

Selection of Studies

Studies were obtained through a Web-based search of the PubMed database. The medical subject heading (MeSH) terms “focal cortical dysplasia” and “surgery” were used to capture all publications related to epilepsy surgery for this specific indication (over 400 studies). Data regarding other malformations of cortical development, including tuberous sclerosis, band and nodular heterotopias, hemimegalencephaly, lissencephaly, and schizencephaly, were excluded.40 Formal inclusion criteria consisted of 1) documented FCD within surgically obtained pathological specimens, and 2) disaggregated Engel outcome score data (or a seizure outcome schema that could be roughly mapped to the Engel classification system; for example, those of Hardiman et al.26 and the International League Against Epilepsy5) for the FCD cohort (in studies analyzing patients with multiple seizure etiologies).61 Exclusion criteria were 1) fewer than 10 surgical candidates with FCD (although such a study might include more than 10 surgical candidates overall), and 2) a greater than 25% FCD dual pathology, for example, mesial temporal sclerosis or neoplasm with FCD in the same surgical specimens, without disaggregation of seizure outcome data for the FCD-only cohort (Table 2). Studies analyzing patients with multiple seizure etiologies without disaggregation of factors other than seizure outcome for the FCD-only cohort were included. Overall, 6 studies were excluded for lack of disaggregated seizure outcome data.4,6,13,46,47,50 Finally, a single study was chosen from serial studies of the same patient cohort when overlap between cohorts was not clearly disambiguated.18–20,34–38,59,60 Thirty-seven studies met all criteria (Table 1).1,8–10,12,14–16,20–25,28–34,36,38,39,42,48,49,51–58,60,62

TABLE 2:

Formal inclusion and exclusion criteria for FCD study selection

Inclusion CriteriaExclusion Criteria
documented FCD w/in surgically obtained pathological specimensstudies w/ <10 FCD surgical candidates
disaggregated seizure outcome scores for FCD cohorts>25% FCD dual pathology w/o disaggregation of seizure outcome data for FCD-only cohort

Data Classification

In statistical analyses, FCD pathology was classified according to the Palmini system.50 Similar designations within the Barkovich et al.,2 Brannstrom et al.,7 International League Against Epilepsy,5 and Mischel et al.44 systems were mapped onto equivalent Palmini categories. This was also done for heuristic classification systems.34,39,55,57,58 In 11 studies, the pathological classification system was not delineated.9,10,16,21–25,28,34,62 Acceptable alternate terms for “focal cortical dysplasia” were “cortical dysgenesis,” “microdysgenesis,” and “cortical microdysplasia” when the pathology described matched that of the Palmini system.31 Moreover, in some studies, “architectural” FCD referred to FCD Type I and “cytoarchitectural” FCD referred to FCD Type II. Data describing mild malformation of cortical development, electrocorticography, and reoperations for recurrent or persistent FCD were excluded from analysis because of inconsistent presentation. Studies were not excluded based on year of publication. In 6 studies, Engel Classes I and II were combined for statistical purposes.8,24,25,28,34,51

Meta-Analysis Methodology

Meta-analyses constitute a class of statistical techniques designed to address inherent differences across populations. We used an algorithm by Lipsey and Wilson41 that calculates a mean effect size weighted by inverse variance (that is, it accounts for differences in study population size) as well as a corresponding 95% confidence interval for a single variable measured across studies. The algorithm accounts for interstudy heterogeneity by treating the dichotomous groups as categorical variables and partitioning within- and between-study variability analogous to continuous variables in the 1-way ANOVA (http://mason.gmu.edu/~dwilsonb/ma.html). Using this algorithm, confidence intervals based on standardized mean effect sizes can be directly compared between categorical variables. Nonoverlapping confidence intervals indicate statistically significant different groups (confidence intervals generated from mean effect sizes not shown). For ease of interpretation, mean effect sizes were transformed into odds ratios with 95% confidence intervals to represent the relationship among the dichotomous comparisons with respect to seizure freedom. Statistical significance was thresholded at p < 0.05. Homogeneity of groups was assessed by the Q index. As regards the 7 variables chosen, 12 of the 14 dichotomous groups exceeded the threshold for expected variability across studies, and thus the majority of our analysis consisted of comparisons among heterogeneous populations (Table 3). Furthermore, internal reliability between studies was below 70% according to the Cronbach alpha statistic (data not shown). To address these constraints, a full-information maximum likelihood random-effects model was used in estimating confidence intervals. Finally, seizure-freedom results from a single study were indentified as an outlier;48 however, analysis results were not changed when data from this single study were excluded given its relatively small patient population.

TABLE 3:

Comparison of perioperative factor groups with respect to seizure outcome following surgery for FCD*

FactorOdds RatiosHomogeneity Assessment
kOR−95% CI+95% CIdfQ1Q2
significant
 partial vs generalized seizures101.461.181.82915.5745.67
 temporal vs extratemporal location201.351.131.6119141.3393.03
 abnormal vs normal MRI141.671.332.161356.0065.01
 FCD Type II vs Type I171.381.221.571635.8969.85
 complete vs incomplete resection153.913.035.321464.6149.34
not significant
 age ≥18 vs <18 yrs131.140.961.351295.56139.85
 unilat vs bilat ictal EEG localization101.030.821.31953.5111.04

* df = degrees of freedom; k = number of studies out of 37 reporting factor; Q = Homogeneity Index (subscripts indicate groups).

† Homogeneous distribution.

Our results are of course subject to selection and other biases inherent to meta-analysis methodologies for which we are unable to control, although we have constructed objective and conservative inclusion and exclusion criteria to capture null studies that balance positive ones to the greatest extent possible (Table 2).

Data associated with 7 variables—seizure type, seizure location, detection with MRI, EEG localization, age at surgery, completeness of resection, and FCD histology type—were separated into dichotomous groups for comparison, as discussed above. Specifically, we compared partial versus generalized seizures, temporal versus extratemporal lobe epilepsy, normal versus abnormal MRI findings, regional localization of ictal onset by EEG versus inability of EEG to localize regional ictal onset, age at surgery < 18 versus ≥ 18 years, complete versus incomplete resection, and FCD Type I versus Type II with regard to seizure freedom in all groups. These variables encompassed the most frequently analyzed factors among previous studies and were chosen for this reason (Table 1). Thresholds were determined based on standard groupings in the literature. Data for individual variables were not included if dichotomous groups could not be formed; for example, we did not include an analysis between age and seizure freedom in a study in which all patients were under the age of 18 years. We defined seizure freedom as an Engel Class I outcome at the latest follow-up defined in each study.17 We included secondarily generalized seizures in the generalized seizures cohort. The median and mean ages were treated similarly. Localization of ictal onset by EEG was considered regional when occurring in a single hemisphere without regard to size of the locus. Localization of ictal onsets and/or resection encompassing both temporal and extratemporal lobes in the same patient were counted as an extratemporal location. Positive MRI findings and completeness of resection were defined by objective neuroanatomical criteria in each study.

All analyses were performed using SPSS version 19 software (IBM Corp.). The Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines were carefully followed.45

Results

We analyzed 2014 patients from 37 studies reporting seizure outcomes following the resection of FCD lesions. The results from these studies were highly variable, and the predictive value of pre- and postoperative factors with regard to seizure freedom was inconsistent (Table 1).

Our analysis showed that, as a group, partial seizures are significantly more often associated with Engel Class I outcomes as compared with generalized seizures (OR 1.46, 95% CI 1.18–1.82; Table 3). A temporal location also portended a higher probability of seizure freedom than did an extratemporal location (OR 1.35, 95% CI 1.13–1.61). Furthermore, an abnormal MRI finding suggestive of FCD was associated with a higher rate of seizure freedom as compared with a normal MRI result (OR 1.67, 95% CI 1.33–2.16). A clear distinction between FCD Types I and II existed with regard to seizure-free outcomes, with more severe pathological features predicting a higher probability of seizure freedom (OR 1.38, 95% CI 1.22–1.57). Finally, patients undergoing complete versus incomplete resections of anatomic or electrographic abnormalities represented the largest, significant difference with respect to seizure-free outcomes (OR 3.91, 95% 3.03–5.32), confirming the results of many studies in this cohort (Fig. 1).

Fig. 1.
Fig. 1.

A forest plot of odds ratios for complete versus incomplete resection calculated from individual studies. Symbols represent the value of the odds ratio on the x axis for a particular study, and symbol sizes are linearly scaled by population study size. The x axis is logarithmically scaled. The overall odds ratio for the comparison of complete versus incomplete resection is denoted by a hashed line at 3.91 on the x axis. Individual studies are labeled on the y axis.

The mean age at surgery averaged across studies for our cohort was 15.4 ± 8.3 years. Using dichotomous groups separated at 18 years of age, we found no difference between these 2 age groups with respect to seizure outcome (OR 1.14, 95% CI 0.96–1.35; Table 3). Electroencephalographic identification of an ictal onset zone also did not appear to have any difference with regard to seizure outcome at the last follow-up (OR 1.03, 95% CI 0.82–1.31).

Discussion

The demographic and perioperative factors associated with postsurgical seizure freedom are inconsistent among published FCD series. We analyzed 7 variables—seizure type, seizure origin, EEG localization, MRI structural abnormalities, age at surgery, completeness of resection, and histopathological FCD type—with respect to seizure freedom to statistically determine factors predictive of an Engel Class I outcome. Using meta-analysis methodology to account for interstudy heterogeneity and population size differences, we found that partial seizures, a temporal location, positive findings on MRI scans, complete margins of resection, and histological FCD Type II were significantly associated with a seizurefree outcome, whereas age at surgery and the ability of EEG to localize epileptogenic regions did not affect the probability of a seizure-free outcome.

Although FCD is the most common etiology of medically refractory epilepsy in children and the third most common in adults, only 5%–10% of all focal epilepsy cases worldwide can be definitively traced to FCD.3,27 Thus, the efficacy of various presurgical assessments, including electrophysiological and imaging modalities, as well as surgical techniques, ranging from lesionectomy to hemispherectomy, has been challenging to characterize in a standardized manner.

While our analyses are limited by the abundance of retrospective, nonrandomized data cohorts in the literature, our methodology and conclusions provide an approach to understanding unresolved issues in the literature that will hopefully begin to be addressed by future prospective studies. Because of inconsistencies in reporting retrospective and often incompletely disaggregated data, we are unable to analyze interactions among variables that might yield further insight into the dynamics of these variables and how they determine, whether directly or indirectly, seizure freedom. As an example, one important variable not included in our analysis was invasive electrocorticographic recordings that may turn out to have an impact on seizure freedom. Our present analyses are therefore strictly univariate, although we predict that significant interactions will probably be discovered in a more robust multivariate model. In addition to more standardized data collection and analysis techniques for these studies, randomized designs should be introduced to more carefully define the benefit of various epilepsy surgery interventions for FCD.

Regardless of etiology, the detectability and resectability of functional and structural abnormalities related to FCD appear to be the most critical determinants of seizure freedom. Advancements in both noninvasive imaging and invasive recordings will likely improve the overall outcomes for patients with intractable epilepsy related to FCD.

Conclusions

Focal cortical dysplasia results from an early disturbance in the migration and final architecture of immature cortical neurons. Because of the disorder's inherent complexity, studies of factors related to surgery for FCD have failed to identify a consistent set of variables that predict postoperative seizure freedom. We have used meta-analytical techniques that reduce interstudy heterogeneity and weight results by population size to statistically identify factors associated with a higher probability of seizure control. We showed that milder semiology, a temporal lobe location, and factors that facilitate the detection of dysplastic lesions, including positive MRI findings and histological FCD Type II, leading to complete resection of the lesion, were significantly associated with a seizure-free outcome. Patient age and the ability of EEG to localize epileptogenic regions did not affect the probability of a seizure-free outcome. Focal cortical dysplasia is a complex, multifactorial condition; however, advances in imaging and surgical modalities have the potential to further improve long-term outcomes.

Disclosure

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author contributions to the study and manuscript preparation include the following. Conception and design: Chang. Acquisition of data: Rowland, Cage, Englot. Analysis and interpretation of data: Rowland, Englot, Sughrue. Drafting the article: Rowland. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Chang. Statistical analysis: Rowland, Englot, Sughrue. Administrative/technical/material support: Cage.

Acknowledgment

The authors thank Dr. Annette Molinaro for her attention to the statistical and mathematical details of the manuscript.

Portions of this work were presented as an oral presentation at the American Association of Neurological Surgeons Conference in 2011.

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    Tassi LPasquier BMinotti LGarbelli RKahane PBenabid AL: Cortical dysplasia: electroclinical, imaging, and neuropathologic study of 13 patients. Epilepsia 42:111211232001

  • 57

    Taylor DCFalconer MABruton CJCorsellis JA: Focal dysplasia of the cerebral cortex in epilepsy. J Neurol Neurosurg Psychiatry 34:3693871971

  • 58

    Urbach HScheffler BHeinrichsmeier Tvon Oertzen JKral TWellmer J: Focal cortical dysplasia of Taylor's balloon cell type: a clinicopathological entity with characteristic neuroimaging and histopathological features, and favorable postsurgical outcome. Epilepsia 43:33402002

  • 59

    Widdess-Walsh PJeha LNair DKotagal PBingaman WNajm I: Subdural electrode analysis in focal cortical dysplasia: predictors of surgical outcome. Neurology 69:6606672007

  • 60

    Widdess-Walsh PKellinghaus CJeha LKotagal PPrayson RBingaman W: Electro-clinical and imaging characteristics of focal cortical dysplasia: correlation with pathological subtypes. Epilepsy Res 67:25332005

  • 61

    Wieser HGBlume WTFish DGoldensohn EHufnagel AKing D: ILAE Commission Report. Proposal for a new classification of outcome with respect to epileptic seizures following epilepsy surgery. Epilepsia 42:2822862001

  • 62

    Wyllie EComair YGKotagal PBulacio JBingaman WRuggieri P: Seizure outcome after epilepsy surgery in children and adolescents. Ann Neurol 44:7407481998

Article Information

Address correspondence to: Edward F. Chang, M.D., Department of Neurological Surgery, University of California, San Francisco, 505 Parnassus Avenue, M-779, San Francisco, California 94143-0112. email: ChangEd@neurosurg.ucsf.edu.

Please include this information when citing this paper: published online February 10, 2012; DOI: 10.3171/2012.1.JNS111105.

© AANS, except where prohibited by US copyright law.

Headings

Figures

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    A forest plot of odds ratios for complete versus incomplete resection calculated from individual studies. Symbols represent the value of the odds ratio on the x axis for a particular study, and symbol sizes are linearly scaled by population study size. The x axis is logarithmically scaled. The overall odds ratio for the comparison of complete versus incomplete resection is denoted by a hashed line at 3.91 on the x axis. Individual studies are labeled on the y axis.

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