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Keywords:

  • IAP;
  • Wada test;
  • Temporal lobe epilepsy

Abstract

  1. Top of page
  2. Abstract
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. REFERENCES

Summary: Purpose: The aim of this study was to compare the utility of baseline neuropsychological measures and scores from the intracarotid amobarbital procedure (IAP) in the prediction of postoperative memory decline in temporal lobe epilepsy surgery patients.

Methods: Logistic regression analyses were used to determine the relation between demographic variables, baseline neuropsychological scores, and scores from the IAP (using mixed verbal and nonverbal stimuli) and postoperative deterioration in verbal learning and verbal recall in 91 patients (48 right, RTL; 43 left, LTL) who had undergone a standard anterior temporal lobe resection for the relief of medically intractable epilepsy and who had been followed up 1 year postoperatively.

Results: In the RTL group, the IAP scores were not significant predictors of a postoperative decline in verbal learning or recall. In the LTL group, postoperative decline in verbal learning was associated with good preoperative baseline scores, an older age at the time of surgery, and an unexpected asymmetry on the IAP. Baseline neuropsychological scores and scores from the IAP were associated with a significant postoperative decline in verbal recall in the LTL group.

 Conclusions: Scores from the IAP using mixed stimuli were not helpful in the prediction of postoperative verbal memory decline in RTL patients. The significance of IAP scores in predicting verbal memory deficits in LTL patients may be task specific.

An ongoing debate exists regarding the future of the intracarotid amobarbital procedure (IAP) (van Emde, 1999; Medina et al., 2004; Duncan et al., 2005; Helmstaedter, 2005; Kirsch et al., 2005; Kloppel and Buchel, 2005). Traditionally, the IAP played an important primary role in the assessment of amnesic risk and is the gold standard against which newer language-lateralizing paradigms are measured (Baxendale, 2002). Data from the IAP have also been used to confirm the lateralization of the seizure focus (Lancman et al., 1998; Lee et al., 2002; Cohen-Gadol et al., 2004). More recently, IAP scores have been used in the statistical modelling of postoperative memory decline (Jokeit et al., 1997; Stroup et al., 2003; Kirsch et al., 2005).

However, these primary and secondary roles have been challenged by new, noninvasive technologies. Patients who “fail” an IAP may not always be at risk of a postoperative amnesic syndrome (Lacruz et al., 2004). Loring et al. (1990) reported 10 such cases who proceeded to surgery, none of whom became amnesic postoperatively. Structural and functional MRI scans can now ensure the integrity of the contralateral structures preoperatively and provide valuable data regarding amnesic risk (Lencz et al., 1992; Baxendale et al., 1998; Kapur and Prevett, 2003; Woermann et al., 2003; Richardson et al., 2004; Janszky et al., 2005; Koepp and Woermann, 2005). In addition, functional imaging paradigms are also proving useful in both the lateralization and localization of specific language functions (Matthews et al., 2003; Sullivan and Detre, 2005). As these techniques begin to supersede the IAP in its traditional roles within the presurgical evaluation, clinical and research emphases have shifted toward the importance of the IAP in the prediction of postoperative memory change (Stroup et al., 2003; Kirsch et al., 2005).

A number of studies have investigated the relation between preoperative IAP scores and postoperative memory function (Loring et al., 1990; Kneebone et al., 1995; Bell et al., 2000; Chiaravalloti and Glosser, 2001; Stroup et al., 2003; Kirsch et al., 2005; Lee et al., 2005). Collectively these studies suggest that the IAP provides valuable prognostic data for memory decline in both adults and children, particularly with respect to verbal memory decline after a left temporal lobe resection (Kneebone et al., 1995; Bell et al., 2000; Chiaravalloti and Glosser, 2001). Stroup et al. (2003) found that IAP scores, side of surgery, preoperative memory function, and underlying pathology were all significantly and independently associated with memory outcome after a temporal lobe resection for epilepsy. Further, the IAP scores were more potent predictors than baseline neuropsychological measures.

As an invasive and expensive procedure, the IAP must be shown to contribute uniquely valuable data to the presurgical evaluation of epilepsy patients if it is to continue to play an important role in epilepsy surgery. Although IAP scores may predict postoperative memory decline, the “added value” of IAP scores over and above other readily available noninvasive indices of risk has yet to be established.

The aim of this study was to compare the contributions of baseline neuropsychological measures with mixed-stimuli IAP scores in the prediction of verbal memory decline in patients who underwent an anterior temporal lobe resection. The focus of this study is solely on the role of the IAP in the prediction of postoperative memory decline, rather than language lateralization or the determination of amnesic risk.

METHODS

  1. Top of page
  2. Abstract
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. REFERENCES

Subjects

The inclusion criteria for the study were all patients who had undergone a successful IAP by using mixed stimuli as part of their surgical evaluation prior to 1995 and who had neuropsychological follow-up 1 year after a right (RTL) or left (LTL) temporal lobe resection for intractable epilepsy at our centre. Patients who did not proceed to surgery were excluded from the study, as were patients who had other than a standard anterior temporal lobe resection (for example, frontal resections and lesionectomies). Patients with atypical language representation were also excluded from the study. Ninety-one patients fulfilled these criteria for our study (48 RTL, 43 LTL). The demographic and clinical characteristics of the RTL and LTL groups are presented in Table 1. No significant differences were found between the RTL and LTL groups in age at the time of surgery, age at onset of seizures, overall level of intellectual function (Verbal & Performance IQ), and preoperative verbal learning and recall.

Table 1. Demographic, clinical, and neuropsychological characteristics of the RTL and LTL groups
 RTL (n = 48)LTL (n = 43)
Gender24 men14 men
24 women29 women
Age at surgery (yr)Median, 29.5 yr (range, 16–51)Median, 30.0 yr (range, 16–48)
Age at seizure onset (yr)Median, 9.5 yr (range, 1–27)Median, 12.0 yr (range, 1–40)
Verbal IQ (SD)93.0 (14.2)92.2 (14.7)
Performance IQ94.8 (14.2)98.8 (14.7)
Preoperative Verbal Learning (max, 75)43.5 (8.4) 43.3 (8.4) 
Postoperative Verbal Learning (max, 75)44.4 (9.4) 38.5 (8.9) 
Preoperative Verbal Recall (max, 15)8.26 (2.7) 8.03 (3.2) 
Postoperative Verbal Recall (max, 15)9.0 (2.8) 6.4 (2.6)
IAP Ipsilateral Hemisphere score5.9 (1.2) 7.2 (0.9)
IAP Contralateral Hemisphere score7.7 (0.7) 7.1 (0.9)
IAP Asymmetry Index1.8 (1.5)−0.17 (1.2)

Patients were selected for temporal lobe surgery after the multidisplinary evaluation of data from the clinical history, neuroradiologic, and neurophysiologic investigations (ictal and interictal), the ictal semiology, neuropsychological assessment, and the IAP. No patients were excluded from the surgical option solely on the basis of adverse IAP data.

Sampling bias

From 1988 to 1995, we conducted 188 standard IAPs by using mixed verbal and nonverbal stimuli. In 1995, we revised the practice of conducting the IAP on all temporal lobe epilepsy surgical candidates. From 1995, the IAP procedure was no longer indicated if the baseline neuropsychology, MRI, and EEG studies all suggested concordant data. All patients in this study underwent surgery prior to 1995. The patients in this study therefore had no sampling bias because all patients underwent the IAP as part of their presurgical evaluation at that time.

Mixed-stimuli IAP protocol

We previously described our mixed-stimuli IAP protocol (Baxendale et al., 1996; 1997). In summary, the hemisphere ipsilateral to the suspected seizure focus was always injected first. The contralateral IAP was performed 45 min later in the same angiography session. An initial dose of 75 mg of amobarbital was administered and followed up with incremental doses of 25 mg until a hemiplegia was produced. Immediately after the injection, the patient was presented with eight items (four verbal and four visual). With the effects of the drug still apparent, they were presented with four of these items again, together with four foils, and are asked whether they recognise them from earlier in the session. On recovery, they are presented with the remaining four original items, with four additional foils, and again asked to identify the items as original or novel.

Procedural failures and complication rate

In 1991, one patient failed the ipsilateral IAP because of edema in the contralateral temporal lobe after an intracranial EEG study. After this case, all IAPs were conducted before intracranial EEG studies. Procedural failures are defined as any event that prohibits or impedes the accurate assessment of memory function during the IAP. These events range from excessive sedation to behavioral disturbance such as marked perseveration, perceptual disturbance, emotional lability, or impaired comprehension. Procedural failures may also be neuroradiologic in nature, such as difficulties with cannula placement or excessive crossflow. Procedural failures occurred in 5.3% of the patients who had undergone the procedure. These patients were excluded from the study. No patients developed a permanent neurologic deficit after an IAP at our centre.

Ipsilateral Hemisphere Score

The Ipsilateral Hemisphere Score refers to the total number of original items recognized (maximum, eight) after injection into the hemisphere contralateral to the suspected seizure focus. To correct for response bias and guessing, we incorporated a correction for each patient by subtracting half of the false-positive responses from the total correctly identified (Baxendale et al., 1996).

Contralateral Hemisphere Score

The Contralateral Hemisphere Score refers to the total number of original items recognized (maximum, eight) after injection into the hemisphere ipsilateral to the suspected seizure focus. As with the ipsilateral score, to correct for response bias and guessing, we incorporated a correction for each patient by subtracting half of the false-positive responses from the total correctly identified (Baxendale et al., 1996).

Asymmetry indices

The IAP Asymmetry Index was calculated by subtracting the Ipsilateral Hemisphere Score from the Contralateral Hemisphere Score. A negative IAP Asymmetry Index suggests that the memory capacity of the hemisphere with the suspected seizure focus is greater than that of the supposed intact hemisphere. An unexpected asymmetry is defined as an Ipsilateral Hemisphere Score greater than the Contralateral Hemisphere Score.

Neuropsychological measures

The List Learning task from the Adult Memory and Information Processing Battery (AMIBP) was used as our measure of verbal memory, as one of the most frequent postoperative memory complaints reported in the clinic is that of a reduction in the ability to take in new material, particularly in conversation. Thus the test has high face validity for the patient population. It also has high test–retest reliability.

We reported the characteristics of the test previously (Baxendale and Thompson, 2005). In summary, the list-learning task was chosen because it shares a similar structure with the California Verbal Learning Test frequently quoted in the international literature, but it has British norms. In the task, the patient is read a list of 15 common words, some of which are semantically related, and asked to recall as many as possible. The total number of words recalled over five trials gives the Verbal Learning Score (max, 75). The subjects are then distracted with a second list of 15 words and asked to recall as many as possible. After the distraction task, they are asked to recall as many as possible from the original list, giving the Verbal Retention Score (max, 15).

Postoperative decline

We previously reported reliable change indices (RCIs) for the list-learning task (Baxendale and Thompson, 2005). The RCI (80%) of the Verbal Learning Score is 10 points. All patients with a postoperative score ≥10 points lower than their preoperative score were classified as having experienced a significant postoperative decline. The RCI (80%) of the Verbal Retention Score is 2.9 points. All patients with a preoperative score ≥3 points higher than their postoperative score were classified as having experienced a significant postoperative decline.

Statistical analyses

The RTL and LTL groups were analysed separately. Logistic regression analyses (stepwise entry with p < 0.05 to enter and 0.10 to exit) were used to determine which variables influenced postoperative memory decline. The following variables were entered into the equation:

  • 1
    Age (years)
  • 2
    Age at onset of habitual epilepsy (years)
  • 3
    Preoperative score
  • 4
    IAP Ipsilateral Hemisphere Score
  • 5
    IAP Contralateral hemisphere Score
  • 6
    IAP Asymmetry Index

A cutoff of 0.25 probability was used to determine which patients were most at risk of a postoperative decline. Although detailed neuroimaging data were available for some of our patients, because of the time scale of the study (1988–1995), imaging data from the earlier patients in the series were not comparable to those available for the patients later in the series. Neuroradiologic indices were therefore not included in the analysis.

RESULTS

  1. Top of page
  2. Abstract
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. REFERENCES

RTL vs. LTL group differences

The LTL group had significantly lower postoperative verbal learning and recall scores than the RTL group (p < 0.01). The LTL group had significantly higher IAP ipsilateral hemisphere memory scores and significantly lower IAP contralateral hemisphere memory scores than the RTL group (p < 0.01). The RTL group also had significantly higher positive (expected) asymmetry scores than the LTL group (p < 0.01).

Verbal learning

Thirty-four of the 91 patients experienced a significant postoperative decline in verbal learning (RTL 13/48; LTL 21/43). In the RTL group, only two patients had an unexpected asymmetry score on the IAP. Neither experienced a postoperative decline in verbal learning. In the LTL group, 20 patients had an unexpected asymmetry score on the IAP. Of these, nine experienced a significant postoperative decline in verbal learning.

LTL group: logistic regression analyses

Postoperative deterioration in verbal learning was significantly associated with the following factors; good preoperative memory function (p < 0.01), older age at the time of surgery (p < 0.05), and the IAP Asymmetry Score (p < 0.05). The model correctly classified all but three (91%) of those who experienced a significant postoperative decline in verbal learning. See Table 2.

Table 2. Regression model characteristics for the RTL and LTL GROUPS: verbal learning vs. verbal recall
 Verbal learningVerbal recall
  1. aReduced model excluding significant IAP variables.

  2. Hit rate, the number of correct predictions per sample size; sensitivity, percentage of patients who declined correctly identified by the model; specificity, percentage of patients who did not decline correctly identified by the model.

Model characteristics (using a cutoff of 0.25)RTL group (n = 48)LTL group (n = 43)RTL group (n = 48)LTL group (n = 43)
Decline (n = 13)Decline (n = 21)  Decline (n = 6)Decline (n = 14)  
Hit rate64.6%62.8% (60.5%)a87.5% 
76.7% (67.4 %)a
Sensitivity76.9%90.5% (100%)a66.7%92.9% (85.7%)a
Specificity60.0%36.4% (22.7%)a90.5% 
69% (58.6 %)a
False-positive rate58% 50%40% (50%)a
42% (44.7%)a 
False-negative rate14.2%20% (0%)a5% 
4% (10%)a
Significant predictor variables (in order of significance)1. Higher age at onset1. Higher preoperative score1. Higher preoperative score1. Lower right hemisphere memory score
2. Negative IAP asymmetry score2. Higher preoperative score
3. Older age at time of surgery3. Higher left hemisphere memory score
4. Greater unexpected asymmetry score.

When the IAP Asymmetry Score was excluded from the analysis, the reduced model including older age at the time of surgery and preoperative score correctly identified 100% of the patients who experienced a postoperative decline, but had a high false-positive rate (44%). See Table 2.

RTL group: logistic regression analyses

In the RTL group, only the age at onset proved a significant predictor of postoperative decline in verbal learning (p < 0.05). Age at the time of surgery and the IAP scores were not significant predictors. The preoperative verbal learning score just failed to reach significance (p = 0.05). The model correctly classified all but three (77%) of those who experienced a significant postoperative decline in verbal learning. See Table 2.

Verbal recall

Twenty of the patients experienced a significant postoperative decline in verbal recall (RTL, n = 6; LTL, n = 14). Neither of the two RTL patients with an unexpected asymmetry score on the IAP experienced a postoperative decline in verbal recall. Of the 20 LTL patients who had an unexpected asymmetry score on the IAP, eight experienced a significant postoperative decline in verbal learning.

LTL group: logistic regression analyses

Postoperative deterioration in verbal recall was significantly associated with the following factors: good preoperative memory function (p < 0.05), a higher IAP ipsilateral hemisphere score (p = 0.01), a lower IAP contralateral hemisphere score (p = 0.05), and a negative IAP asymmetry index (p = 0.05). The model correctly classified all but one (93%) of those who experienced a significant postoperative decline in verbal learning. See Table 2.

When the IAP scores were excluded from the analysis, the reduced model including just the preoperative score correctly identified 86% of the patients who experienced a postoperative decline, but had a high false-positive rate (50%). See Table 2.

RTL group: logistic regression analyses

In the RTL group, only the preoperative verbal learning score was a significant predictor of postoperative decline in verbal learning (p = 0.05). Age at seizure onset and at the time of surgery and the IAP scores were not significant predictors in the equation. The model correctly classified four of the six patients who experienced a significant postoperative decline in verbal learning. See Table 2.

DISCUSSION

  1. Top of page
  2. Abstract
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. REFERENCES

Our results suggest that an IAP using mixed stimuli provides different data for RTL and LTL groups. The confounding effects of language laterality mean that LTL patients have significantly higher ipsilateral hemisphere scores and lower contralateral hemisphere scores than the RTL patients. As a result, LTL patients are far more likely to have an unexpected asymmetry score than are RTL candidates. These findings suggest that it is inappropriate to equate the mixed-stimuli IAP ipsilateral/contralateral hemisphere memory scores of RTL and LTL groups. These findings support Jokeit's (2004) contention than the IAP data from RTL and LTL groups must be analyzed separately in regression analyses using IAP data.

The mixed-stimuli IAP scores were not significant predictors of a postoperative decline in verbal learning or recall in our RTL group. Consistent with previous findings, we found that higher baseline neuropsychological scores and an older age at seizure onset were significant predictors of decline in verbal recall and learning in this group (Chelune et al., 1991; Hermann et al., 1995; Jokeit et al., 1997; Davies et al., 1998). However, the mixed-stimuli IAP scores were significant predictors of postoperative decline in both verbal learning and recall in the LTL group. An unexpected IAP asymmetry score, together with an older age at the time of surgery and good preoperative functioning were significant predictors of postoperative decline in verbal learning. All of the IAP indices were significant predictors of a postoperative decline in verbal recall, together with higher baseline scores. Although the sensitivity of the model increased when the IAP asymmetry score was excluded in the prediction of a postoperative decline in verbal learning, this was at the expense of specificity. In our data set, the IAP asymmetry score increased the specificity of the model in predicting significant postoperative decline in verbal learning in LTL patients, over models including simple demographic data and baseline neuropsychological scores. Similarly, the addition of our mixed-stimuli IAP indices increased both the sensitivity and specificity of the model used to predict postoperative decline in verbal recall, over the model based simply on baseline neuropsychological scores in LTL patients.

It is possible that the significance of the IAP variables in predicting postoperative verbal memory decline may be due to an artifact. The LTL patients are more likely to decline on verbal memory measures postoperatively and are also more likely to have unexpected IAP asymmetry scores because of the confounds of language dominance. Thus the verbal stimuli used in our IAP may be significant factors in the results. Further work is under way to investigate the relation between IAP scores derived from a different IAP protocol using real objects as memory stimuli and postoperative decline in verbal memory.

This study has a number of limitations that constrain the conclusions that can be drawn from the data. Our sample included only patients who were left hemisphere dominant for language. Intracarotid amobarbital procedures vary greatly in methods and materials. This protocol uses a mixture of both verbal and nonverbal stimuli, and we always injected the side of the suspected seizure onset first, introducing the possibility of a small, but systematic, “second injection” effect on memory performance. The measures of verbal memory include a measure of learning and immediate recall but not delayed recall. These limitations should be borne in mind when considering the clinical implications of our findings outlined later.

Clinical implications

After the introduction of fMRI paradigms to the clinical investigation of epilepsy surgery patients, the role of the IAP has increazingly come into the spotlight. The traditional roles of the IAP in lateralizing language and in screening for amnesic risk are being superseded in the presurgical evaluation of epilepsy patients by structural and functional MRI scans. Although no doubt exists that the IAP can provide lateralizing and prognostic data, the added value of the data must be carefully assessed to justify using an invasive and expensive procedure. Our findings suggest that the prognostic value of our mixed-stimuli IAP data in predicting postoperative memory change is very limited in left hemisphere language-dominant RTL patients. As such, it is difficult to justify the application of such an IAP in these patients solely to gain prognostic data to predict postoperative deterioration in verbal learning and recall.

Statistically, our mixed-stimuli IAP indices provided superior data to baseline neuropsychological scores in the prediction of postoperative decline in our LTL patients. However, in practical terms, the models including IAP indices enabled the identification in just one additional patient who was at risk of a postoperative decline in verbal recall, and just four LTL patients were correctly reclassified at low risk in our sample, of a denominator of 43, 21 of whom had a decline in verbal memory.

In our view, this refinement of prediction does not justify the use of the mixed-stimuli IAP in all LTL patients solely to gain prognostic data to predict postoperative deterioration in verbal learning and recall. This raises ethical and economic issues about the “added value” of mixed-stimuli IAP data in the prediction of postoperative change in LTL patients. These can be addressed partly by examining the use to which postoperative prediction are put. It is important that every patient be given as much information as possible regarding the risks of a temporal lobe resection to their memory function, to enable them to make an informed decision before surgery. However, whether a statistical definition of deterioration is clinically meaningful for a given patient will depend on many factors, including the nature and extent of his environmental demands and, to some extent, his or her psychosocial resources and support systems (Baxendale et al., 2006). It is extremely difficult for patients to weigh precise statistical likelihoods in the surgical decision-making process. The difference between a 60% chance and a 65% chance of an event occurring is unlikely to alter the decision-making process. Thus the added value of these IAP scores in improving the prediction of postoperative memory decline may have negligible clinical relevance for the patient. In addition, because generally a poor correlation is found between objective measures of memory function and patients' complaints (Baxendale and Thompson, 2005), even if our IAP data did improve the accuracy of a predictive model, the clinical relevance of the information to the patient might well be outweighed by the invasive nature of the procedure.

In addition, now other noninvasive indices of structure and function can be used to predict postoperative memory decline in both RTL and LTL groups (Hermann et al., 1995; Jokeit et al., 1997; Davies et al., 1998; Baxendale et al., 2006). Because of the historical nature of the sample, it was not possible to include quantitative or qualitative indices from structural or functional MRI studies in this study that have been shown to be significant predictors of postoperative memory change.

The IAP has often been cited as the “gold standard” in the assessment of language lateralization and in the screening for amnesic risk of prospective temporal lobe surgery patients. However, it has not been established as the gold standard for the prediction of postoperative memory decline. A number of other demographic and clinical factors have also been shown to be associated with postoperative memory decline, the majority of which can be quantified by using noninvasive methods. Whereas it makes sense to use IAP measures where they are already available to predict postoperative memory decline, our results suggest that it is not appropriate to conduct an invasive mixed-stimuli IAP solely to gain prognostic data regarding postoperative memory decline.

REFERENCES

  1. Top of page
  2. Abstract
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. REFERENCES
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