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September 01, 1999; 53 (4) Article

Patient-oriented outcome assessment after temporal lobectomy for refractory epilepsy

F. Gilliam, R. Kuzniecky, K. Meador, R. Martin, S. Sawrie, M. Viikinsalo, R. Morawetz, E. Faught
First published September 1, 1999, DOI: https://doi.org/10.1212/WNL.53.4.687
F. Gilliam
From the Departments of Neurology (Drs. GilliamKuzniecky, Martin, Sawrie, and Faught, and M. Viikinsalo) and Neurosurgery (Dr. Morawetz), UAB Epilepsy Center, University of Alabama-Birmingham; and the Department of Neurology (Dr. Meador), Medical College of Georgia, Augusta, GA.
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R. Kuzniecky
From the Departments of Neurology (Drs. GilliamKuzniecky, Martin, Sawrie, and Faught, and M. Viikinsalo) and Neurosurgery (Dr. Morawetz), UAB Epilepsy Center, University of Alabama-Birmingham; and the Department of Neurology (Dr. Meador), Medical College of Georgia, Augusta, GA.
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K. Meador
From the Departments of Neurology (Drs. GilliamKuzniecky, Martin, Sawrie, and Faught, and M. Viikinsalo) and Neurosurgery (Dr. Morawetz), UAB Epilepsy Center, University of Alabama-Birmingham; and the Department of Neurology (Dr. Meador), Medical College of Georgia, Augusta, GA.
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R. Martin
From the Departments of Neurology (Drs. GilliamKuzniecky, Martin, Sawrie, and Faught, and M. Viikinsalo) and Neurosurgery (Dr. Morawetz), UAB Epilepsy Center, University of Alabama-Birmingham; and the Department of Neurology (Dr. Meador), Medical College of Georgia, Augusta, GA.
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S. Sawrie
From the Departments of Neurology (Drs. GilliamKuzniecky, Martin, Sawrie, and Faught, and M. Viikinsalo) and Neurosurgery (Dr. Morawetz), UAB Epilepsy Center, University of Alabama-Birmingham; and the Department of Neurology (Dr. Meador), Medical College of Georgia, Augusta, GA.
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M. Viikinsalo
From the Departments of Neurology (Drs. GilliamKuzniecky, Martin, Sawrie, and Faught, and M. Viikinsalo) and Neurosurgery (Dr. Morawetz), UAB Epilepsy Center, University of Alabama-Birmingham; and the Department of Neurology (Dr. Meador), Medical College of Georgia, Augusta, GA.
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R. Morawetz
From the Departments of Neurology (Drs. GilliamKuzniecky, Martin, Sawrie, and Faught, and M. Viikinsalo) and Neurosurgery (Dr. Morawetz), UAB Epilepsy Center, University of Alabama-Birmingham; and the Department of Neurology (Dr. Meador), Medical College of Georgia, Augusta, GA.
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E. Faught
From the Departments of Neurology (Drs. GilliamKuzniecky, Martin, Sawrie, and Faught, and M. Viikinsalo) and Neurosurgery (Dr. Morawetz), UAB Epilepsy Center, University of Alabama-Birmingham; and the Department of Neurology (Dr. Meador), Medical College of Georgia, Augusta, GA.
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Citation
Patient-oriented outcome assessment after temporal lobectomy for refractory epilepsy
F. Gilliam, R. Kuzniecky, K. Meador, R. Martin, S. Sawrie, M. Viikinsalo, R. Morawetz, E. Faught
Neurology Sep 1999, 53 (4) 687; DOI: 10.1212/WNL.53.4.687

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Abstract

Objective: To determine patient-oriented outcome after anterior temporal lobectomy (ATL) for refractory epilepsy.

Background: Health-related quality of life (HRQOL) is an important component of the assessment of outcome from epilepsy surgery, but prior controlled studies of the effect of surgery on HRQOL are inconclusive. Direct assessment of the effect of surgery on patient concerns of living with epilepsy has not been reported.

Methods: We used reliable and valid instruments to compare HRQOL and patient concerns of 125 patients who had received an ATL more than than one year previously to a clinically similar group of 71 patients who were awaiting ATL. All patients were selected for surgery based on similar criteria. We also used bivariate correlation analysis and multivariate regression modeling to determine the association of traditional outcome variables with HRQOL.

Results: Patients who had undergone ATL reported significantly less concern of living with epilepsy in 16 of 20 items of the EFA Concerns Index and better HRQOL in 8 of 11 scales of the Epilepsy Surgery Inventory-55. Regression analysis in the postoperative group demonstrated that mood status, employment, driving, and antiepileptic drug (AED) cessation, but not seizure-free status or IQ, were associated with better HRQOL.

Conclusions: Our findings support a positive affect of ATL on patient concerns and HRQOL in refractory temporal lobe epilepsy, although longitudinal studies are needed to corroborate these results. Mood, employment, driving ability, and AED use are important postoperative predictors of HRQOL.

Assessing outcome from anterior temporal lobectomy (ATL) traditionally has focused on seizure frequency and severity,1 but increased recognition of the complex psychosocial effects of epilepsy has resulted in development of more comprehensive assessments of patient well-being and function.2-8 A recent study demonstrated that reliable and valid measures of health-related quality of life (HRQOL) can assist evaluation of seizure-based outcome classification systems.9 Controlled, prospective investigations of outcome based on HRQOL, however, have not demonstrated significantly better HRQOL in many important domains in the surgically treated group.10-12 These findings are particularly problematic considering the difficulties in completing randomized, controlled trials of outcome from epilepsy surgery.12-14 The two published prospective, controlled, nonrandomized studies of HRQOL after epilepsy surgery used control subjects who were rejected from surgery after extensive evaluation.11,12 These control samples had significantly more preoperative seizures than the surgical groups, and presumably had a more severe disorder, but did not demonstrate inferior HRQOL in most domains during serial evaluations. Vickrey et al.12 reported improvement in surgery patients in one half of the scales assessed by a cross-sectional component of their study. McLachlan et al.11 found no between-group differences in 9 of 11 scales at 12 months follow-up but did demonstrate a difference in 6 scales at 24 months owing to deterioration in the scores of the remaining nonsurgical patients. Additional evidence for improvement in HRQOL after epilepsy surgery is needed to determine standards for quality of care and to refine the informed consent process.3,15,16

The use of HRQOL measures has been criticized because most instruments were not developed using systematic assessment of the patient’s perspective.17,18 After a comprehensive review of studies including HRQOL outcome variables, Gill and Feinstein17 concluded that “quality of life can be suitably measured only by determining the opinions of patients and by supplementing the instruments developed by experts.” The complexity of the psychosocial outcome from epilepsy surgery requires that accurate techniques be used to determine well-being and function from the patient’s perspective.2,3,19-22

We report a study comparing patients’ concerns and HRQOL in a group of patients who had undergone ATL to a clinically similar group with long-standing refractory temporal lobe epilepsy awaiting ATL. We also evaluated conventional clinical outcome variables including seizure frequency, employment status, driving status, verbal and performance IQ, and antiepileptic drug (AED) use to determine their association with HRQOL in the postoperative group.

Methods.

Subjects.

Patients with medically intractable localization-related epilepsy were evaluated for temporal lobectomy at the University of Alabama-Birmingham Epilepsy Center between 1987 and 1996. All patients had complex partial seizures, and most also had a history of secondarily generalized seizures. Medical failure was determined by trials of at least three AEDs incrementally increased to highest tolerable dosages. Most patients had taken four or more different AEDs alone and in combination. Active psychotic disorder or severe mental retardation was a relative contraindication, but surgery was considered in such patients if seizures posed a significant risk of mortality or serious injury. ATL was offered when the presurgical evaluation indicated that seizures arose from one temporal lobe. Patients whose evaluations connoted multiple epileptogenic regions or nontemporal seizure onset were excluded from temporal lobectomy. The criteria for recruitment and selection of patients for presurgical evaluation did not change appreciably during the study period.

For this study the patients were divided into two groups. The first group consisted of all adult patients over 17 years of age who had received an ATL before 1993, and the second group consisted of adult patients selected for ATL in 1995 and 1996. The first group underwent outcome assessment greater than one year after surgery, whereas patients in the second group were selected for ATL but were assessed before receiving surgery.

The presurgical evaluation protocol used MRI, interictal and ictal scalp video/EEG monitoring with sphenoidal or anterior temporal electrodes, and comprehensive neuropsychological testing to identify neurophysiological, structural, and functional abnormalities.23 Our decision process was similar to previously published algorithms.24,25 To summarize briefly, if the MRI demonstrated unilateral hippocampal atrophy or signal changes, and interictal and ictal video/EEG identified unilateral temporal lobe abnormalities and major clinical seizure features that were concordant with the MRI results, the patient was offered an ATL. If the MRI, interictal EEG, or ictal EEG were normal or did not localize to one temporal lobe, intracranial EEG monitoring with bilateral epidural electrode strips placed under both temporal lobes was performed to confirm the location of seizure onset.26 PET and intracarotid sodium amobarbital testing were used to confirm functional deficits in selected patients to provide supportive evidence for lateralization of the epileptogenic region. If intracranial monitoring verified that seizures arose from one mesial temporal lobe, ATL was offered to the patient. The video/EEG monitoring, MRI, and neuropsychological evaluation techniques did not change appreciably during the study period, except that coronal inversion recovery and fluid-attenuated inversion recovery (FLAIR) sequences were added to the MRI protocol in 1993. Informed consent was obtained from each patient before all procedures and before entry into the study using a document approved by our Institutional Review Board.

Surgical technique.

A standard procedure was performed in all patients. A single neurosurgeon performed the most recent 115 resections. The surgical technique did not change during the study period. Dominant resections included the anterior 4 cm of the temporal lobe, and nondominant resections included approximately 5 cm of basal and lateral neocortex, sparing the superior temporal gyrus. The amygdala and anterior 1.5 to 2 cm of the hippocampus were removed.

Development of the Epilepsy Foundation of America (EFA) Concerns Index and HRQOL assessment.

The initial phase of the development of the Concerns Index consisted of systematic assessment of the concerns of 81 patients with chronic epilepsy.7 Each patient was asked to list in order of importance his or her concerns of living with recurrent seizures. The tabulated concerns were transposed into questions that were reviewed for completeness and appropriateness in a series of small-group structured interviews with the same patients. This protocol was designed to minimize the intrusion of investigator bias, as described in detail in a prior publication.7

Based on the results of the prior study,7 we selected items for the EFA Concerns Index presented in figure 1. The domains assessed by these questions involve driving, autonomy, work, education, family, seizure effects, medication effects, mood and anxiety, and social activity. Ratings on each five-point scale are summed, producing a Concerns Index score that ranges from 20 to 100. The following components of the validity testing were assessed in the entire cohort of 196 patients, including both the postoperative and preoperative patients in the present study. The equal weighting of concerns was supported by the similar correlations of individual items with the total score, ranging from 0.65 to 0.85 for all but two items. The high degree of internal-consistency reliability of the index was supported by a value of Cronbach’s α of 0.94; values larger than 0.7 are considered acceptable for group comparisons. Construct validity was supported by the finding that the mean total index scores were significantly less in patients who were seizure free after ATL, compared with those who continued to have complex partial or secondarily generalized seizures (43 versus 54, p < 0.0001). Concurrent or criterion validity was determined by comparison of several individual items to previously validated measures of conceptually similar domains. Question 15 assessing concern about medication side-effects correlated with the Adverse Events Profile27 total score (r = 0.44, p < 0.0001). Question 19 assessing depression and anxiety symptoms correlated with the Profile of Mood States (POMS)28 total score (r = 0.52, p < 0.01). Question 18 assessing memory correlated with the Quality of Life in Epilepsy Inventory29 cognitive functioning scale (r = −0.76, p < 0.01). Test-retest reliability was 0.85 in a separate cohort of 82 epilepsy patients who completed two questionnaires 2 to 3 weeks apart.

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Figure 1. EFA Concerns Index.

We also used the Epilepsy Surgery Inventory (ESI)-5519 to assess HRQOL in the entire cohort. The ESI-55 is a reliable and valid measure developed by Vickrey et al.19 that consists of the SF-3630 and 19 additional epilepsy-specific items. The scale’s possible scores range from 0 to 100. Earlier studies using the ESI-55 indicate that it is a useful external standard that adds outcome information compared with conventional outcome classifications that emphasize seizure frequency as the primary variable.9

Outcome assessment.

Outcome variables included the EFA Concerns Index, ESI-559,12,19 (11 scales and 3 composite scales), seizure frequency, AED use, Adverse Events Profile27 total score (range 19 to 95 with higher scores indicating greater drug effects), POMS28 total score (range -32 to 204 with higher scores indicating worse mood problems), driving status, employment status, and verbal and performance IQ. Seizure frequency, AED use, driving status, and employment status were determined by a mailed questionnaire that also included the EFA Concerns Index, the ESI-55, the Adverse Events Profile, and the POMS. All postoperative patients also completed a structured telephone interview that confirmed demographic, seizure, AED, driving, and employment data. Preoperative seizure rates in the postoperative group were confirmed by chart review to avoid recall errors. The POMS was administered simultaneously so that concerns and HRQOL could be correlated with mood status. Patients in the preoperative group completed the questionnaires during the presurgical evaluation before a final decision regarding surgery. Verbal and performance IQ were measured before and 6 months after ATL using the Weschler Adult Intelligence Scale-Revised.31

For the purposes of this study, patients were considered seizure free if no complex partial or secondarily generalized seizure occurred during the 12 months before outcome assessment. Employment was defined as working >20 hours per week. Full-time students and patients choosing to work in the home were also included in the employed category. Patients working or in school less than part-time, as well as homemakers who considered themselves underemployed, were classified as unemployed. Driving status and AED requirement were also categorized as dichotomous variables.

Data analysis.

The primary outcome measures, the EFA Concerns Index and the ESI-55 mean scale scores, were used to compare postoperative and preoperative groups by analysis of variance performed by SPSS general linear model multivariate analysis, which allowed adjustment for potential covariates, including gender, epileptic region lateralization, preoperative verbal and performance IQ, duration of epilepsy, and education. Clinical outcome measures were compared with the ESI-55 composite scale scores for role function, mental health, and physical health within the postoperative group using Pearson’s correlation coefficient (r for continuous, point-biserial for dichotomous variables) and multivariate stepwise regression analysis. Correlation coefficients of clinical variables with seizure cessation were also obtained. All outcome data were stored and analyzed using a computerized statistical program (SPSS 8.0 for Windows, Chicago, IL).

Results.

One hundred twenty-five patients who had received an ATL more than one year earlier and 71 consecutive preoperative patients selected for ATL were enrolled in the study. The postoperative group consisted of 86% of the total 145 adult patients who underwent ATL before the enrollment period. The 20 patients who did not return adequate outcome data were not significantly different from the surgical cohort in terms of seizure control and AED use, thus decreasing the risk of selection bias as presented in table 1. One of these patients had died before outcome assessment. The preoperative characteristics for the entire cohort of both groups of patients are shown in table 2; no statistically significant differences were found between groups in age at epilepsy onset, gender, lateralization of the epileptogenic zone, duration of epilepsy, seizure frequency, IQ, or education.

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Table 1.

Comparison of clinical variables in the preoperative group, postoperative group, and postoperative group with incomplete outcome data

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Table 2.

Preoperative characteristics of the entire cohort of patients who received an anterior temporal lobectomy (ATL) or who were awaiting an ATL

Figure 2 presents the comparison of Concerns Index scores between the presurgical and postsurgical groups. All concerns except those regarding other people’s poor understanding of epilepsy, obtaining work or education, being treated unfairly, and finding transportation were significantly less in the patients who had undergone ATL.

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Figure 2. Comparison of EFA Concerns Index scores in patients selected for anterior temporal lobectomy (ATL) and those >1 year after ATL. ▪ = Pre-ATL (n = 71); ⋄ = Post-ATL (n = 125). Lower score = less concern. General linear model multivariate analysis of variance (ANOVA), which controlled for the covariates gender, epileptic region lateralization, preoperative verbal and performance IQ, duration of epilepsy, and education, demonstrated a difference between groups significant at a p value <0.05 for all items except 5, 8, 13, and 20.

Figure 3 shows the comparison of ESI-55 scale scores between the two groups. All scales except physical function, overall quality of life, and pain were significantly better in the postoperative group.

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Figure 3. Comparison of Epilepsy Surgery Inventory-55 scale scores in patient groups before and >1 year after anterior temporal lobectomy (ATL). ▪ = Pre-ATL (n = 71); ⋄ = Post-ATL (n = 125). HP = health perception; E/F = energy/fatigue; OQOL = overall quality of life; SF = social function; EWB = emotional well-being; CF = cognitive function; RL-E = role limitations-emotional; RL-M = RL-memory; RL-P = RL-physical; PF = physical function. Higher scores = better HRQOL. General linear model multivariate ANOVA, which controlled for the covariates gender, epileptic region lateralization, preoperative verbal and performance IQ, duration of epilepsy, and education, demonstrated a difference between groups significant at a p value <0.05 in all scales except physical function, OQOL, and pain.

Table 1 summarizes the clinical variables assessed in the preoperative and postoperative groups. In the post-ATL group, 65% of patients were seizure free or had only auras during the past year, 60% were driving, 62% were employed or in school, and 30% took no AEDs. Twenty-two (18%) post-ATL patients who were seizure free did not drive, and 12 (10%) admitted to driving despite continued complex partial seizures. In the pre-ATL group, 61% were employed or in school. The Adverse Events Profile and POMS mean total scale scores were significantly worse in the preoperative group. Preoperative verbal IQ and performance IQ were similar in both groups.

The Pearson’s product-moment coefficients for continuous independent variables and the Pearson’s point-biserial coefficients for dichotomous independent variables are presented in table 3 for each of the dependent variables of Mental Health, Physical Health, and Role Function ESI-55 composite scale scores. The correlation coefficients indicated significant associations of all dependent variables with mood status, employment, driving, and AED use. Physical Function and Role Function composite scales were significantly correlated with cessation of seizures, although the coefficients were smaller than the other associated clinical variables. The absolute correlation coefficients for seizure cessation with clinical variables listed in table 3 ranged from 0.026 (postoperative performance IQ) to 0.391 (driving), indicating no strong associations.

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Table 3.

Bivariate Pearson’s correlation coefficients for ESI-55 Composite Scale scores with clinical variables within the postoperative group (n = 125)

Table 4 presents the results of the stepwise regression analysis comparing ESI-55 composite scale scores of role function, mental health, and physical health (dependent variables) to the independent variables. Mood status, employment, driving, and AED use explained 37% to 59% of variance within the composite HRQOL scales. Mood status was most closely associated with all ESI-55 composite scale scores, whereas seizure-freedom and verbal and performance IQ were not significantly associated with any composite scores.

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Table 4.

Final stepwise regression models for the association of Epilepsy Surgery Inventory (ESI)-55 composite scales with conventional clinical variables (n = 125)

Discussion.

Our study used the HRQOL instrument designed for epilepsy surgery outcome assessment that was used in prior controlled studies,11,12 but the design also included a reliable and valid measure of patients’ concerns. This study also used a control group of patients who were selected for ATL after a standardized presurgical evaluation. We found that most domains of HRQOL were significantly better in the postoperative group. The two previous controlled studies of HRQOL outcome after epilepsy surgery did not find this extent of between-group differences.11,12 However, the prospective exploratory component of the study by Vickrey et al.12 used a generic HRQOL measure that may not have been sensitive to changes in epilepsy-specific HRQOL. More similar to our results, the cross-sectional component of their study using the ESI-55 demonstrated better scores in the surgical group in one half of the instrument’s scales; our groups differed on all of these scales except pain.12 McLachlan et al.’s investigation of ATL is difficult to compare with our study; their calculated overall ESI-55 scores improved by about 12% from baseline in both the surgical and medical control groups at 6- and 12-month assessments, but deterioration in the remaining 13 controls allowed for a significant difference between groups at 24 months.11 The improvement in controls during the initial phase of their study suggests the possibility that the increased intensity of overall care often administered during the surgical consideration period, such as more frequent clinic visits and psychosocial services, may improve HRQOL independent of surgical intervention.

The cross-sectional design of our study may be a significant limitation because it does not control for the potential confounders associated with surgical intervention (e.g., placebo effect), selection bias, or the possible improvement of a nonsurgical control group over time when treated in a comprehensive epilepsy center. Alternative study designs using prospective, nonrandomized medical controls or presurgical assessments as controls, however, do not eliminate selection bias or confounding effects potentially associated with surgery. An earlier study did partially address the issue of a potential surgical placebo effect; the Penfield and Jasper surgical series demonstrated that 18/65 (28%) of a “sham” control group that received an exploratory craniotomy without cerebral resection experienced a significant seizure reduction.32 The study was performed when very limited medical options were available and did not include psychosocial assessment. Some authors have reported deterioration or no change in HRQOL over time in patients with refractory temporal lobe epilepsy,11,33 although HRQOL improved in the medical controls during the first 12 months in one of these studies.11 Most of our control group had received care at our center for at least one year before entering the study and were presumably experiencing optimal medical improvement, but the interaction with medical personnel probably intensified during the period of the surgical evaluation.

Some health services researchers have emphasized the necessity of including direct patient assessments in the process of HRQOL outcome determination. We agree with Gill and Feinstein17 who have proposed that “devising suitable creative strategies to ascertain, incorporate, and weigh patients’ preferences is one of the fundamental intellectual challenges facing quality-of-life researchers today.” Leplege and Hunt18 further emphasized that “the argument that it is the patients who are replying to questions designed by experts is not sufficient to claim that the scores … reflect the patients’ viewpoint.” Our findings indicate that the concerns expressed specifically by patients living with refractory epilepsy were significantly less in the ATL group and were concordant with better HRQOL.

When HRQOL measures are used as an external standard to evaluate conventional clinical variables, the results differ from common assumptions about the relative importance of seizure cessation compared with the psychosocial effects of epilepsy. The regression model in our sample indicated that postoperative mood, employment, driving, and medication use, but not seizure cessation or IQ, predict HRQOL. Results of the correlation analysis comparing the strength of association of clinical variables with seizure cessation and with ESI-55 composite scores suggest that the ranking of clinical variables in the regression model is not determined by collinearity with seizure cessation. Other studies also have reported disparity of seizure outcome with psychosocial status and satisfaction in certain groups of patients.6,10,34 These observations do not diminish the importance of freedom from seizures but highlight the complex configuration of influences that epilepsy has on the well-being and function of individuals. For example, HRQOL may be better in patients who are experiencing seizures but maintaining employment compared with patients who are seizure free but not employed. It is also possible that improvement is bidirectional; better HRQOL may allow improved mood, employment, and autonomous activity. Our findings still suggest that additional intervention through vocational rehabilitation, transportation services, antidepressant or anxiolytic therapy, and minimization of drug side effects may significantly improve HRQOL, independent of seizures.

Further prospective, controlled comparisons of surgical and psychosocial (e.g., mood, employment, transportation, AED effects) intervention may aid our understanding of the complex effects of epilepsy and its surgical treatment. Although a randomized controlled trial comparing outcome from ATL to optimal medical management is unlikely to be performed for logistical and ethical reasons, our results provide controlled clinical data to support a positive effect of surgery on patient concerns and HRQOL in medically refractory temporal lobe epilepsy. We have demonstrated concordance of patient-oriented measures of concerns and HRQOL, both of which appear sensitive to effects of surgical intervention in patients with recurrent seizures.

Acknowledgments

Supported by National Institutes of Health grant NS01794-01 and a research grant from the Epilepsy Foundation of America.

Footnotes

  • See also page 662

  • Received September 22, 1998.
  • Accepted in final form June 3, 1999.

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