Memory outcome after left anterior temporal lobectomy in patients with expected and reversed Wada memory asymmetry scores

PURPOSE: The ideal candidate for anterior temporal lobectomy surgery shows a Wada memory asymmetry (WMA) score characterized by better memory performance in the hemisphere contralateral to the seizure focus relative to the ipsilateral (surgical) hemisphere. However, some surgical candidates show a reversed WMA or better Wada memory performance in the hemisphere of surgical interest relative to the hemisphere contralateral to the seizure focus. To date, no data are available contrasting memory and seizure outcome for these two Wada groups. The present study compared memory and seizure outcome after left anterior temporal lobectomy (L-ATL) in patients showing expected and reversed WMA scores, and also examined the relationship of the individual hemisphere Wada memory scores for predicting verbal memory outcome after L-ATL. METHODS: We compared 6-month postoperative verbal memory change scores and seizure outcome in L-ATL patients with either an expected (n=12) or reversed WMA (n=9) pattern on Wada memory testing. RESULTS: L-ATL patients showing a reversed WMA score had a poorer verbal memory outcome and poorer seizure control after surgery compared with patients showing a WMA score in the expected direction. CONCLUSIONS: L-ATL patients with a reversed WMA score have a greater risk for memory morbidity and poorer seizure outcome than do patients with a WMA score in the expected direction. The WMA score was the best predictor of memory outcome after L-ATL. When the WMA score is not considered, both individual Wada hemisphere scores (contralateral and ipsilateral) provided significant and independent contribution to predicting postoperative verbal memory functioning. These findings are discussed in the context of the functional reserve and hippocampal adequacy models of memory change after temporal lobectomy.     

The Wada memory test and prediction of outcome after anterior temporal lobectomy

We reviewed the records of 77 Chinese-speaking adult patients to investigate the relationship between the Wada memory test and outcomes after anterior temporal lobectomy (ATL). The ipsilateral memory scores, contralateral memory scores and Wada asymmetry index (WAI) were calculated to evaluate their relationships with seizure and cognitive outcomes. The seizure outcomes did not correlate with the unilateral memory scores or the WAI. Patients who had a smaller WAI tended to have a post-operative decline in verbal intelligence quotient (VIQ) (odds ratio: 13.54, 95% confidence interval: 1.17–156.11, p = 0.037). The seven patients who failed the Wada memory test after ipsilateral injection had a higher percentage of VIQ deterioration than the 70 who passed (p = 0.039). However, no patient displayed global amnesia after surgery. The Wada memory test was a predictor for post-operative VIQ changes in our study. Patients who failed the Wada memory test still benefitted from the ATL and showed good seizure outcomes.     

Memory outcome 2 years after anterior temporal lobectomy in patients with drug-resistant epilepsy

PURPOSE: Memory decline is often observed after anterior temporal lobectomy (ATL), particularly in patients with dominant hemisphere resections. However, the follow-up length has been 1 year or less in most studies. Our aims were to examine postoperative memory changes over a longer period and to identify baseline demographic and clinical predictors of memory outcome. METHODS: We administered material-specific memory tests at baseline, and 1 and 2 years after surgery to 82 consecutive right-handed patients (52% males) who underwent ATL for drug-resistant temporal lobe epilepsy (TLE) (35 left, 47 right) after a non-invasive presurgical protocol. Repeated measures multivariate analysis of variance (RM-MANOVA) was used to examine the relationship between changes in memory tests scores over time and side of TLE and pathology. Also, standardized residual change scores were calculated for each memory test and entered in multiple linear regression models aimed at identifying baseline predictors of better memory outcome. RESULTS: RM-MANOVA revealed a significant change in memory test scores over time, with an interaction between time and side of surgery, as 2 years after surgery patients with RTLE were improved while patients with LTLE were not worse as compared with baseline. Pathology was not associated with changes in memory scores. In multiple regression analysis, significant associations were found between right TLE and greater improvement in verbal memory, younger age and greater improvement in visuospatial memory, and male gender and greater improvement in both verbal and visuospatial memory. CONCLUSIONS: Our results suggest that the long-term memory outcome of TLE patients undergoing ATL without invasive presurgical assessment may be good in most cases not only for right-sided but also for left-sided resections.     

Effects of dual pathology on cognitive outcome following left anterior temporal lobectomy for treatment of epilepsy

The objective of this retrospective study was to determine if dual pathology [DUAL — focal cortical dysplasia (FCD) and mesial temporal sclerosis (MTS)] in patients with left temporal lobe epilepsy is associated with greater risk for cognitive decline following temporal lobectomy than single pathology (MTS only). Sixty-three adults (M_age = 36.5 years, female: 52.4%) who underwent left anterior temporal lobectomy for treatment of epilepsy (MTS = 28; DUAL = 35) completed preoperative and postoperative neuropsychological evaluations. The base rate of dual pathology was 55.5%. Repeated measures ANOVAs yielded significant 2-way interactions (group × time) on most measures of language and memory with generally moderate effect sizes. Specifically, patients with MTS only demonstrated postoperative declines, while those with dual pathology remained unchanged or improved. Results suggest that dual pathology may be associated with better cognitive outcome following epilepsy surgery than MTS alone, possibly reflecting limited functionality of the resected tissue or intrahemispheric reorganization of function in the context of a developmental lesion.     

Outcome of patients with early postoperative seizures following anterior temporal lobectomy

Retrospective analysis of the records of patients with postoperative seizures immediately following anterior temporal lobectomy was performed to identify variables predictive of outcome. The data indicate that the absence of epileptiform activity on the postoperative scalp EEG is a strong predictor of good outcome. A young age at seizure onset is a weaker, but significant and additive, predictor of good outcome. There is also a trend for patients having early generalized seizures to have better outcomes than those having early complex partial seizures. There is no predictive value in age at operation, sex, or postoperative electro-corticography, nor does outcome in patients with mass lesions differ from patients without mass lesions.     

Neuropsychological effects associated with temporal lobectomy and amygdalohippocampectomy depending on Wada test failure

OBJECTIVE: To compare the neuropsychological effects of temporal lobectomy (TL) and amygdalohippocampectomy (AH), depending on whether the patients had passed or failed the Wada test. METHODS: We compared changes in neuropsychological scores in patients who underwent TL (n = 91) or AH (n = 15), and had passed or failed the Wada test. Comparisons were carried out in all 106 patients and among the 20 patients who failed the Wada test (12 who had TL and 8 who had AH). RESULTS: No patient became globally amnesic after surgery. Among all patients, no differences were found in pre-surgical or change scores (percentage of change after surgery compared with preoperative values) of neuropsychological tests between patients who underwent TL or AH. Among patients who failed the Wada test, those in the TL group showed higher visual memory impairment (p<0.05). There was a strong trend suggesting that TL is associated with higher verbal memory deficits than AH (p = 0.07). Of those TL patients who failed the Wada test, the contralateral Wada score correlated with change scores in verbal intelligence quotient (p<0.01), and there was a strong trend towards a correlation with the logical memory immediate recall version subtest of the Wechsler Memory Scale (p = 0.06). CONCLUSIONS: No profound changes in intelligence quotient or memory scores were found after TL or AH. Nevertheless, patients who underwent TL and failed the Wada test showed more deficits than those who passed the test or those who had AH. The presence of a correlation between contralateral Wada scores and verbal deficits in TL patients who failed the Wada test but not among AH patients suggests that, if temporal surgery is required, AH might be preferred to TL in patients who fail the Wada test.     

Lateralized seizure termination: relationship to outcome following anterior temporal lobectomy.

Determination of side of seizure onset is critical for a successful outcome following epilepsy surgery. Little is known about the significance of lateralized seizure termination. Sustained seizure activity contralateral to side of seizure onset, following termination of ictal activity ipsilateral to side of onset, may suggest the presence of an independent focus. Such activity, if present, should predict a poor outcome. We studied side of seizure termination in 13 patients undergoing monitoring with bitemporal depth electrodes and correlated this to outcome following anterior temporal lobectomy (ATL). Side of seizure onset was determined for all seizures during that evaluation. Based on side of final cessation of ictal activity, patients were classified as having ipsilateral final termination or simultaneous termination (Group 1; N=6) or contra-lateral or mixed final termination (Group 2; N=7). The Duke outcome classification system was used. At the end of 2 years follow-up, 6/6 patients in Group 1 and 3/7 patients in Group 2 were seizure free. We conclude that lateralized seizure termination during evaluation with depth electrodes may be useful in predicting outcome following ATL. Continued seizure activity contralateral to side of seizure onset (following termination of ictal activity ipsilateral to side of onset) predicts a poor outcome. This may indicate the presence of an independent seizure focus opposite to the side of surgery.     

Factors predicting seizure outcome of anterior temporal lobectomy for patients with mesial temporal sclerosis.

PURPOSE: To investigate the factors, including those associated with ictal scalp EEG results, related to surgical outcome in patients with pathologically proven mesial temporal sclerosis. METHODS: We studied 51 consecutive patients who underwent anterior temporal lobectomy and had at least 4 years of follow-up. Surgical outcome was classified as being seizure-free or not seizure-free during the first two and the subsequent two postoperative years. Clinical variables and scalp EEG parameters were subjected to statistical analysis. RESULTS: Of the 51 patients, 36 (70.6%) were seizure-free during postoperative years 3 and 4. Logistic regression analysis revealed that seizure remission for the first 2 years (p = 0.002) and contralateral propagated ictal discharges (p = 0.015) were independently related to seizure outcome at 4 years. Patients who were seizure-free at 2 years had an 86.5% chance of remaining seizure-free at 4 years. Of the patients without bitemporal asynchrony or switch of lateralization, 88.9% were seizure free at 4 years, compared with 54.5% of patients with asynchrony or switch of lateralization (p = 0.007). These two factors, however, were not predictive of seizure outcome at 2 years. CONCLUSIONS: Contralateral propagated ictal discharges, including bitemporal asynchrony and switch of lateralization, unfavorably influence long-term seizure outcome. Long-term seizure control is best when the patient has no such propagation patterns of ictal discharges and is seizure-free during the first 2 years after temporal lobectomy.     

Validation of the WMS-III Facial Memory subtest with the Graduate Hospital Facial Memory Test in a sample of right and left anterior temporal lobectomy patients

A number of studies have shown visuospatial memory deficits following anterior temporal lobectomy (ATL) in the right, nondominant temporal lobe (RATL). The current study examines 26 patients with intractable temporal lobe epilepsy who underwent ATL in either the right (RATL, n = 16) or left temporal lobe (LATL, n = 10) on two tests of facial memory abilities, the Wechsler Memory Scale-III (WMS-III) Faces subtest and the Graduate Hospital Facial Memory Test (FMT). Repeated measures ANOVA on the FMT indicated a significant main effect of side of surgery. The RATL group performed significantly below the LATL group overall. Both groups showed a slight, but non-significant, improvement in performance from pre- to postsurgery on the FMT immediate memory, likely due to practice effects. Repeated measures ANOVA on the WMS-III Faces subtest revealed a significant interaction of group (RATL vs. LATL) by delay (immediate vs. delayed). Overall, the LATL group showed an improvement in recognition scores from immediate to delayed memory, whereas the RATL group performed similarly at both immediate and delayed testing. No effects of surgery were noted on the WMS-III. Following initial data analysis the WMS-III Faces I and II data were re-scored using the scoring suggested by Holdnack and Delis (2003), earlier in this issue. Repeated measures ANOVA revealed a trend toward significance in the three-way interaction of group (RATL vs. LATL) x time of testing (pre- versus postop) x delay (immediate vs. delayed memory). On the Faces I subtest, both the RATL and LATL groups showed a decline from preoperative to postoperative testing. However, on Faces II the LATL group showed an increase in performance from preoperative to postoperative testing, while the RALT group showed a decline in performance from preoperative to postoperative testing. While the FMT appears to be superior to the WMS-III Faces subtest in identifying deficits in facial memory prior to and following RATL, the application of the scoring methodology presented by Holdnack and Delis earlier in this issue does serve to increase the clinical utility of the WMS-III Faces subtest in this population.     

Short-term neurocognitive outcomes following anterior temporal lobectomy

Changes in cognitive function are a well established risk of anterior temporal lobectomy (ATL). Deficits in verbal memory are a common postoperative finding, though a small proportion of patients may improve. Postoperative evaluation typically occurs after six to 12 months. Patients may benefit from earlier evaluation to identify potential needs; however, the results of a formal neuropsychological assessment at an early postoperative stage are not described in the literature. We compared pre- and postoperative cognitive function for 28 right ATL and 23 left ATL patients using repeated measures ANOVA. Changes in cognitive function were compared to ILAE seizure outcome. The mean time to postoperative neuropsychological testing was 11.1 weeks (SD = 6.7 weeks). There was a side × surgery interaction for the verbal tasks: immediate memory recall (F(1,33) = 20.68, p < 0.001), short delay recall (F(1,29) = 4.99, p = 0.03), long delay recall (F(1,33) = 10.36, p = 0.003), recognition (F(1,33) = 5.69, p = 0.02), and naming (F(1,37) = 15.86, p < 0.001). This indicated that the left ATL group had a significant decrement in verbal memory following surgery, while the right ATL group experienced a small but significant improvement. For the right ATL group, there was a positive correlation between ILAE outcome and improvement in immediate recall (r = − 0.62, p = 0.02) and long delay recall (r = − 0.57, p = 0.03). There was no similar finding for the left ATL group. This study demonstrates that short-interval follow-up is effective in elucidating postoperative cognitive changes. Right ATL was associated with improvement in verbal memory, while left ATL resulted in a decrement in performance. Improvement in the right ATL group was related to improved seizure outcome. Short-interval follow-up may lend itself to the identification of patients who could benefit from early intervention.     

Olfactory memory in patients with anterior temporal lobectomy.

Right and left temporal lobectomy patients, matched in age and intelligence, made more errors in odor recall than a control group. Patients with right temporal lobe excisions recalled significantly fewer odors correctly than patients with left temporal lobe excisions. Olfactory memory scores were not related to other memory deficits associated with left or right temporal lobe dysfunction or to intelligence or lesion size. However, in patients with right temporal lobectomy, percent of odors recalled correctly correlated positively with a general memory index. The findings presented are consistent with previous reports that the right temporal lobe is more involved with nonverbal memory than the left temporal lobe.     

Preserved proper naming following left anterior temporal lobectomy is associated with early age of seizure onset

PURPOSE: Anterior temporal lobectomy (ATL) is an effective surgical option for managing pharmacoresistant temporal lobe epilepsy. Many patients with left ATL develop postsurgical difficulties with proper name retrieval, although curiously, some patients have entirely intact proper naming following left ATL. Here, we tested the hypothesis that early age of seizure onset would be a reliable factor "protecting" patients from developing proper naming defects following left ATL. METHODS: Proper naming of unique persons (Famous Faces Test, 155 items) and places (Landmark Test, 65 items) was measured in 23 patients who had undergone left ATL for pharmacoresistant epilepsy. Data were collected for a number of variables, including age of seizure onset, age at surgery, handedness, IQ, and seizure outcome. The patients were sorted into two groups based on proper naming performance: (1) Unimpaired: 7 patients performed normally on both the Faces and Landmark tests; (2) Impaired: 16 patients performed abnormally on one or both of the tests. RESULTS: In support of our hypothesis, the Unimpaired group had a significantly earlier age of seizure onset (M = 2.1 years) than the Impaired group (M = 15.1 years). Moreover, a correlation analysis indicated a strong association between age of seizure onset and naming outcome (R =-0.569). The groups were comparable (and statistically indistinguishable) on nearly all other variables. CONCLUSIONS: These findings document the importance of age of seizure onset in predicting proper naming outcome following left ATL (with earlier being better), and extend understanding of brain reorganization and plasticity.     

Risk to verbal memory following anterior temporal lobectomy in patients with severe left-sided hippocampal sclerosis

BACKGROUND: Previous investigations indicate low risk for memory loss following anterior temporal lobectomy (ATL) in patients with severe hippocampal sclerosis (HS) compared with patients with mild HS. However, these conclusions have been established primarily with group-level analyses. OBJECTIVE: To investigate individual base rate risk for verbal memory loss following ATL in patients who have pathologically verified mild, moderate, or severe HS. PATIENTS AND METHODS: One hundred fifteen patients with unilateral temporal lobe epilepsy (68 with left-sided and 47 with right-sided epilepsy) were included. Acquisition, retrieval, and recognition components of verbal memory, as measured by the California Verbal Learning Test, were assessed before and after ATL. Postoperatively, the degree of neuronal loss and reactive gliosis of the hippocampus was assessed via a 3-tiered rating system establishing mild, moderate, and severe pathologic features. Patients with preoperative magnetic resonance imaging-based evidence of lesions outside the mesial temporal area (side of surgical resection) were excluded. RESULTS: Neither seizure laterality nor severity of HS was associated with preoperative verbal memory performance. Postoperatively, the left-sided ATL group demonstrated significant decline across the acquisition (P<.01), retrival (P<.001), and recognition (P<.001) verbal memory components compared with the right-sided ATL group. Patients who underwent left-sided ATL and had mild HS displayed the largest magnitude and percentage proportion of postoperative decline across all verbal memory components. However, 28 (48%) of the 58 patients who underwent left-sided ATL and who had moderate and severe HS displayed statistically reliable declines on retrieval aspects of verbal memory. Most patients undergoing right-sided ATL, regardless of the extent of hippocampal pathologic features, displayed no postoperative memory change. CONCLUSIONS: Substantial individual heterogeneity of memory outcome exists across groups of patients undergoing ATL, with various degrees of pathologically verified HS. Patients undergoing left-sided ATL who have mild HS seem at greatest risk for broad-spectrum verbal memory decline. However, when examining outcome on a patient-by-patient basis, many patients undergoing left-sided ATL who have moderate to severe HS were also vulnerable to verbal memory loss. This risk seems selective to a retrieval-based aspect of verbal memory.     

Seizure outcome after anterior temporal lobectomy and its predictors in patients with apparent temporal lobe epilepsy and normal MRI

PURPOSE: Very little reliable information is available regarding the role of anterior temporal lobectomy (ATL), optimal presurgical evaluation strategy, post-ATL seizure outcome, and the factors that predict the outcome in patients with medically refractory temporal lobe epilepsy (TLE) and normal high-resolution magnetic resonance imaging (MRI). To be cost-effective, epilepsy surgery centers in developing countries will have to select candidates for epilepsy surgery by using the locally available technology and expertise. METHODS: We reviewed the electroclinical and pathological characteristics and seizure outcome of 17 patients who underwent ATL for medically refractory TLE after being selected for ATL based on a noninvasive selection protocol without the aid of positron emission tomography (PET) or single-photon emission computed tomography (SPECT), despite a normal preoperative high-resolution MRI. RESULTS: Seven (41%) patients achieved an excellent seizure outcome; five of them were totally seizure free. An additional five (29%) patients had >75% reduction in seizure frequency. The following pre-ATL factors predicted an excellent outcome: antecedent history of febrile seizures, strictly unilateral anterior temporal interictal epileptiform discharges (IEDs), and concordant type 1 ictal EEG pattern. All the five patients with pathologically verified hippocampal formation neuronal loss were seizure free. The presence of posterior temporal, bilateral temporal, and generalized IEDs portended unfavorable post-ATL seizure outcome. CONCLUSIONS: A subgroup of patients destined to have an excellent post-ATL outcome can be selected from MRI-negative TLE patients by using history and scalp-recorded interictal and ictal EEG data. The attributes of these patients are antecedent history of febrile seizures, strictly unilateral anterior IEDs, and concordant type 1 ictal EEG pattern.     

Predictors of postoperative memory function after left anterior temporal lobectomy

Patients who undergo left anterior temporal lobectomy (ATL) for intractable epilepsy are at risk of postoperative memory decline. This study attempts to identify the best predictors of memory after ATL using preoperative tests. Thirty-two consecutive patients who underwent left ATL with preoperative and postoperative neuropsychological testing were retrospectively identified. The following independent variables were analyzed by multiple regression: age of onset of seizures, age of temporal lobe damage, gender, MRI results, preoperative memory testing, and intracarotid amytal procedure (IAP) results. Neuropsychological measures of verbal and nonverbal memory served as dependent variables. Male gender (P<0.005), failing the IAP with both left and right hemispheres (P<0.001), and higher logical memory (LM) scores preoperatively (P<0.001) were associated with greater declines in LM after surgery. Our data demonstrate that the IAP predicts postoperative memory independent of other factors known to affect memory after left ATL.     

Presurgical electroencephalographic patterns and outcome from anterior temporal lobectomy.

We reviewed data from 48 patients after anterior temporal lobe resection for medically intractable epilepsy. All had ictal electro-encephalographic (EEG) evidence of unilateral temporal lobe onset. Depth electrodes were used in 19 patients. Successful surgical outcome correlated significantly with factors that suggested a temporal lobe focus, particularly in the interictal scalp EEG. The most successful outcome occurred in patients with well-localized unilateral interictal temporal spikes (100% improved). The group with well-localized bilateral temporal spikes also did well (76% improved). Patients with extratemporal spread of the interictal spike on scalp EEG, either unilaterally or bilaterally, did less well. Only one third improved, despite extensive extracranial and intracranial monitoring, when indicated. The interictal scalp EEG may be the only EEG necessary for the presurgical evaluation of selected patients with intractable temporal lobe epilepsy.