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Verbal Fluency in Focal Epilepsy: A Systematic Review and Meta-analysis

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Abstract

Testing of verbal fluency is currently part of standard presurgical neuropsychological assessment for patients with focal epilepsy. However, to date no systematic review has been conducted on semantic (SVF) and phonemic verbal fluency (PVF) in this patient group. The present review compares verbal fluency between healthy control subjects and subgroups of adult presurgical patients with focal epilepsy according to lateralisation and localisation of the dysfunction. PubMed was searched with a comprehensive search string. Abstracts of all studies and full-texts of potentially relevant studies were screened. Study quality was assessed by independent raters according to predefined criteria. 39 studies were included. Meta-analyses were performed to compare SVF and PVF across groups of patients with temporal (TLE) and frontal lobe epilepsy (FLE) as well as healthy controls (HC). Both patients with left- and right sided TLE were impaired on SVF and PVF compared to HC. Patients with left-sided TLE were slightly more impaired than patients with right-sided TLE. Patients with FLE showed a larger impairment in PVF than patients with TLE, whereas on SVF there was no difference between FLE and TLE. For TLE comparisons the study pool seems to have been sufficient, whereas more studies are needed to verify results for FLE. Semantic verbal fluency might not differentiate between FLE and TLE. While verbal fluency impairment was anticipated, especially in left-sided TLE and FLE patients, the impairment in patients with right-sided TLE was larger than expected. Results are discussed with regard to neuropsychological theory and practice.

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Authors and Affiliations

  1. Epilepsy Center, University Medical Center Freiburg, Breisacher Str. 64, 79106, Freiburg, Germany

    B. Metternich, F. Buschmann, K. Wagner & A. Schulze-Bonhage

  2. Department of Medical Psychology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany

    L. Kriston

Authors
  1. B. Metternich
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  2. F. Buschmann
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  3. K. Wagner
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  4. A. Schulze-Bonhage
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  5. L. Kriston
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Correspondence to B. Metternich.

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Metternich and Buschmann, both authors contributed equally to this work.

Appendix

Appendix

Details on study selection

The abstracts of all identified studies were screened by two independent raters according to predefined criteria (see Table 1). Initially, in 99.6 % raters agreed on whether a study was to be included or excluded. The single case of dissent was resolved by discussion. In 80 % there was initial agreement on the exact reasons for exclusion that could be drawn from the abstract, i.e. mostly the number of exclusion reasons provided differed between raters. Disagreements were resolved by discussion. Full-texts of the studies identified as potentially relevant in the first screening were examined for inclusion by the same independent raters. If important data were missing or insufficiently reported, the corresponding author of the publication was contacted, and in case of a response the provided information was used in the review. Studies judged to be eligible after examination of full-texts represent the study population included in the present review.

Details on assessment of risk of bias

Regarding comparability, the tolerated difference between groups on demographic and clinical variables was half a pooled standard deviation. If data were missing or not reported, this resulted in a negative rating. We weighted the categories listed in the table below according to their considered importance as sources of bias. The quality assessment per criterion was multiplied with the category weight (see table). The resulting figures for each criterion were added up; studies with a sum score of ≥ 1 were considered to bear a low risk of bias. All other studies were classed as being at high risk.

Categories rated in the risk of bias assessment and their assigned weights:

Category

Comparability of groups on IQ/education, duration/onset of epilepsy, age

Comparability of groups on seizure frequency

Comparability of groups on AED

Language dominance measures

Sample size

Recruitment

Blinded assessment of verbal fluency

Quality of outcome measures

Weight

2

1

1

1

1

0,5

0,5

0,5

Scores of −2 to +2 were given for each category and multiplied with the category weight (detailed table available from the authors).

Example: Adcock et al. 2003 (category rating x category weight):

$$ -2\mathrm{x}2+-1\mathrm{x}1+-1\mathrm{x}1+2\mathrm{x}1+-1\mathrm{x}0,5+-1\mathrm{x}0,5+-1\mathrm{x}0,5+-1\mathrm{x}1=-6,5 $$

Sum scores below +1 were classed as high risk of bias.

Details on data synthesis

Using the standardized mean difference as effect measure was necessary because the primary studies assessed the same outcome with several different measures. If not reported by the primary authors, standard deviations were calculated according to the Cochrane Handbook for Systematic Reviews of Interventions (Higgins & Green, 2011). Due to expected clinical and methodological diversity across studies, individual effect sizes were summarized using a random effects model, which assumes that each study estimates different effects that follow a common distribution (DerSimonian and Laird 1986). The subgroup analysis in studies including patients with solely mesiotemporal pathology was pre-specified. Studies reporting data for individual patients were also included here. In these cases we manually extracted the relevant data for patients with mesiotemporal pathology. In order to determine whether the main results were influenced by sources of bias, we conducted a pre-specified subgroup analysis for major comparisons including only studies at low risk of bias. In addition, as one might consider the presence of a healthy control group in a study as a proxy indicator for study quality, we conducted a subgroup analysis for comparisons between diseased groups including only studies with healthy control groups. This analysis followed expert recommendation during the peer-review process and was therefore post hoc. Funnel plots were investigated for comparisons including at least ten studies. Funnel plots are scatter plots displaying results of individual studies along with their precision. If no publication bias is present, this plot should resemble a symmetrical inverted funnel. All analyses were performed using Review Manager 5.1 (Cochrane Collaboration, Copenhagen).

Additional materials, e.g., tables for risk of bias assessment/analyses and forest plots are available from the authors.

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Metternich, B., Buschmann, F., Wagner, K. et al. Verbal Fluency in Focal Epilepsy: A Systematic Review and Meta-analysis. Neuropsychol Rev 24, 200–218 (2014). https://doi.org/10.1007/s11065-014-9255-8

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