The neuropsychological and emotional consequences of living with intractable temporal lobe epilepsy: implications for clinical management

Seizure 2002; 11: 224–230

doi:10.1053/seiz.2001.0668, available online at http://www.idealibrary.com on

The neuropsychological and emotional consequences of living with intractable temporal lobe epilepsy: implications for clinical management PASCALE M. MOORE & GUS A. BAKER The Walton Centre for Neurology and Neurosurgery, Centre for Neurology and Neurosurgery, Liverpool, England Correspondence and reprint requests to: Dr Gus A Baker, The Walton Centre for Neurology and Neurosurgery, Centre for Neurology and Neurosurgery, Lower Lane, Fazakerley, Liverpool, L9 7LJ, England

Purpose: To investigate and document the neuropsychological and emotional effects of epilepsy in people with intractable temporal lobe epilepsy (TLE). Methods: 273 patients with a diagnosis of TLE underwent a complete neuropsychological and psychological examination as a routine part of their investigation for epilepsy surgery. Neuropsychological assessment included measures of intellect, memory, language functioning, higher executive functioning, emotional well-being and the psychosocial impact of epilepsy and its treatment. Results: The sample comprised 135 females and 138 males with a clearly lateralised epileptogenic focus. Patients were mildly anxious but not depressed, although many reported that epilepsy and its treatment had a marked effect on their daily lives. Current reading ability was in the average range; the mean obtained full scale IQ was 88 (low average range). Verbal memory functioning was within the borderline impaired range with visual memory functioning within the average range. Mean language performance was between the 5–10th percentile. Higher executive functioning results were in the normal range. Multiple univariate analyses were performed according to onset laterality. There were no significant differences between the groups on measures of psychological or emotional functioning. Participants with left TLE scored significantly lower than those in the right temporal group on measures of verbal intelligence, general intelligence, attention span and expressive language functioning. Conclusions: Patients with intractable epilepsy suffer significant neuropsychological difficulties in terms of their intellect, memory and language. Higher executive functioning appears unaffected. In addition, there is also evidence of emotional distress. These all impact upon their day-to-day functioning, which can be improved by the application of various psychological therapies and interventions. c 2002 Published by Elsevier Science Ltd on behalf of BEA Trading Ltd.

Key words: epilepsy; neuropsychological; psychological; clinical implications.

INTRODUCTION It is well recognised that people with epilepsy suffer significant psychosocial problems compared to people without epilepsy 1 . These include high levels of anxiety and depression and poor self-esteem. People with epilepsy are more likely to be un- or under-employed, with lower rates of marriage and greater social isolation 2 . They often feel stigmatised by their condition. In addition to coping with the psychosocial consequences, people with epilepsy 1059–1311/02/$22.00/0

also report significant changes in their cognitive functioning with complaints of decreased levels of attention and concentration, poor short-term memory, slowness in thinking and lack of motivation 3 . Recent studies, however, of people with epilepsy in remission report a much more positive psychosocial profile than people with frequent seizures and many patients can lead a full and normal life without significant intellectual decline 4 . Unfortunately for patients with resistant epilepsy, the combined effects of the underlying lesion, uncontrolled seizures and the

c 2002 Published by Elsevier Science Ltd on behalf of BEA Trading Ltd.

Temporal lobe epilepsy: neuropsychological and emotional consequences

continuous use of antiepileptic drug (AED) treatment usually result in impaired neuropsychological functioning that can seriously compromise aspects of their quality of life. As a consequence, neuropsychology has a major role in the assessment and treatment of patients with resistant epilepsy; early identification and documentation of their individual needs should be an essential aspect of their management. Clearly, the precise nature of the impact of chronic, resistant epilepsy and its treatment will vary with the individual. Researchers have reported the following psychological difficulties in epilepsy populations: social isolation 5 , lower sociability and confidence 6 , poor sense of control, psychosis, anxiety and depression 7–9 . Add to these the social problems arising from possessing a diagnosis of a stigmatising disorder: poor living conditions, problems in family and working life, and the heavy emotional burden of living with epilepsy becomes more evident. The neuropsychologist’s input in response to such a list of psychosocial difficulties is often to aid the individual in making a positive adjustment to their epilepsy condition, hopefully resulting in increased compliance, motivation and enhanced adaptation and lifestyle changes. In addition, psychological approaches can aid in the non-pharmaceutical reduction of seizure frequency. In addition to the psychological difficulties associated with medically intractable seizures, there are also significant neuropsychological sequelae including: intellectual decline, memory deficits, language impairment, reduced speed of information processing, compromised levels of attention and concentration and higher executive functioning. Results from studies of people with a well-lateralised temporal lobe seizure focus 10, 11 and those who have undergone surgical resection of the temporal lobes 12 appear to support consistently the generally held view in neuropsychology of lateralised material-specific memory deficits: damage to the left temporal lobe (LTL) leads to difficulties in remembering verbally-presented information, whereas right temporal lobe (RTL) damage adversely affects memory for non-verbal (usually visuospatial) material 13 . However, such clear-cut material-specific findings have not always been replicable and the reasons put forward to explain this relate mainly to inadequacies in testing apparatus, particularly with regard to assessment of visuospatial intellect and memory 14–16 . Researchers in the area are currently investigating and developing new measures, which hopefully will prove to be more reliable and valid in the lateralisation of cognitive deficits in such patients. In addition to lateralisation of seizure focus, several other factors can affect cognitive function in this population over the years. These include the long-term

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administration of AEDs 17, 18 , seizure-related variables (i.e., age of onset/duration of epilepsy disorder, type and severity of seizures) 19 and underlying neuropathology. An early age of seizure onset can be expected to disrupt education and has been related to a lowered verbal IQ on the Wechsler adult intelligence scale-revised (WAIS-R) and reading ability 20 . Although evidence of a cognitive decline has not necessarily been found 21 , other researchers have reported a tendency towards lower verbal IQ scores in people with left hemisphere foci and lower performance IQ in those with right-sided foci 22 . As with memory discrepancies, verbal/performance IQ discrepancies do not consistently distinguish between left and right temporal lobe epilepsy (TLE) patients 14, 23 . The aim of this study was to investigate and document the psychological and neuropsychological effects of epilepsy and its treatment in a cohort of people with intractable left- or right-sided TLE. A further aim was to discuss the implications for clinical management of such patients.

METHODS Patients were hospitalised for investigation of intractable seizure disorders and underwent a complete neuropsychological examination as part of their routine investigation. Table 1 presents the neuropsychological measures that were administered to assess various aspects of cognitive functioning. The NART-R is used principally as a measure to predict the pre-morbid level of intelligence. However, as many people with chronic epilepsy are likely to have begun their seizures peri-natally or during childhood, the relevance of a ‘pre-morbid’ estimate comes into question. Hence, caution should be used when employing the NART-R with an epilepsy population. It is used in our sample as a measure of current reading ability rather than as an estimate of pre-morbid functioning.

Statistical analysis Means, standard deviations and ranges were computed for the whole sample to document the range and variety of emotional and neuropsychological effects of living with intractable TLE. Multiple univariate comparisons were made between participants with documented right and LTL foci to investigate the theory of complementary specialisation between the temporal lobes. Due to the large number of comparisons, we considered applying the Bonferroni factor to account for type I error. The Bonferroni approach

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Table 1: Neuropsychological tests employed. Aspect of emotion/cognition

Measure used

Source

Emotional distress Psychosocial adjustment to epilepsy General intelligence Current reading ability Memory functioning Expressive language functioning—confrontation naming Verbal fluency—by letter Higher executive functioning

Hospital anxiety and depression scale (HADS) Impact of epilepsy scale Wechsler adult intelligence scale-revised (WAIS-R) National adult reading test-revised (NART-R) Wechsler memory scale-revised (WMS-R) Graded naming test

Zigmond and Snaith, 1986 24 Jacoby et al. 1993 25 Wechsler, 1981 26 Nelson, 1991 27 Wechsler, 1987 28 McKenna and Warrington, 1983 29

Benton verbal fluency task Stroop neuropsychological screening test

Lezak, 1983 13 Trenerry et al. 1989 30

relies on a procedure that multiplies the significance result by the number of comparisons made. In this study because of multiple comparisons it would almost be impossible to show any differences, real or not. However, this approach has been acknowledged to be highly conservative and may mask actual differences existing between the two groups. RESULTS There were 273 (135 female and 138 male) patients with a diagnosis of TLE included in our sample. The current study represents an extension to the sample reported upon in previous publications 15, 16 . For all participants, a clear diagnosis of epilepsy was made, based on neuroimaging and electrophysiological records. In all but 80 cases (28% of the total group), a clear epileptogenic focus was identified by experienced consultant neurologists through the use of intensive interictal and ictal EEG recordings with surface or sphenoidal electrodes with concurrent videomonitoring, coupled with clinical and neuropsychological data. No distinction was made on the basis of different aetiologies underlying the epilepsy. Of the 273 patients, 193 had a temporal lobe onset that could be clearly lateralised (Table 2). Patients were included in the left (N = 109) or right (N = 84) temporal groups only if they had exclusively unilateral foci. Table 2: Epilepsy variables. Parameter Site of focus: Left temporal Right temporal Other temporal Medication: Monotherapy Polytherapy: 2 drugs 3 or more drugs Unknown

No. of patients

Percent of group

109 84 80

40 31 29

63

23

117 28

44 9

65

24

The mean age of the sample was 31.8 years, and the mean educational level was 11.8 years. The mean age of onset of epilepsy, determined from the time epilepsy was first diagnosed, was 12.3 years. Mean scores, SD and ranges of the emotional and neuropsychological measures for the whole sample are shown in Table 3. There is evidence for mild levels of anxiety, but no depression is indicated from the HAD scale. The impact of epilepsy score indicates that a significant proportion of participants scored within the upper quartile, indicating that their epilepsy and its treatment were having a significant adverse effect on their day-to-day functioning. An analysis of the WAIS-R scores for the whole group revealed that they were functioning in the low average range of intelligence with no significant verbal/performance discrepancy. Their current reading ability (using the national adult reading test-revised (NART-R)), places them in the average range, across both verbal and non-verbal (visuospatial) abilities. The WMS-R scores were in the low average range for general memory functioning, attention and concentration skills and delayed recall of both verbal and visual material. Immediate recall of visual material was in the average range, whereas verbal memory ability was classified in the borderline impaired range. Confrontation naming performance (using the graded naming test) fell between the 5–10th percentile, indicating some degree of impairment in expressive language functioning. As regards measures of higher executive functioning, a Benton verbal fluency score of 33 is within the normal range and performance on the Stroop test (assessing the allocation of attention) is at the 31st percentile, also within the average range. Multiple univariate analyses were conducted to compare scores across the left and right temporal focus groups (Table 4). There were no significant differences between the two groups in terms of age, years of education or age of epilepsy onset. The two groups are thus comparable with respect to these variables. Only four statistically significant differences

Temporal lobe epilepsy: neuropsychological and emotional consequences

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Table 3: Means, classifications, SDs and ranges for the whole temporal group. Variable

N

Mean score

Classification

SD

Range

HADS: Anxiety Depression

88 88

10.20 6.20

Mild range Normal range

4.65 4.03

1–21 1–21

Impact of epilepsy

33

26.36

Impaired range

7.09

12–40

WAIS-R: Verbal IQ Performance IQ Full scale IQ

255 254 256

90.01 88.52 88.50

Average range Low average Low average

13.38 13.65 12.99

62–129 60–129 60–131

NART-R: Verbal IQ Performance IQ Full scale IQ

236 236 236

98.18 99.20 98.67

Average Average Average

12.18 11.50 12.70

70–126 73–125 67–127

WMS-R: Verbal memory Visual memory General memory Attention/concentration Delayed recall

266 267 267 267 265

79.48 91.88 80.09 87.39 80.51

Borderline Average Low average Low average Low average

14.94 20.16 17.78 19.51 19.01

50–122 50–138 50–125 50–135 50–131

Graded naming score Verbal fluency score Stroop percentile

152 117 85

14.12 33.09 31.56

5–10th percentile Average range Average range

5.43 12.75 8.02

1–26 11–90 1–100

Note: HADS = Hospital anxiety and depression scale; WAIS-R = Wechsler adult intelligence scale-revised; NART-R = National adult reading test-revised; WMS-R = Wechsler memory scale-revised.

QOL

Self esteem

Rel - friends

1 + pm

Health

Seizure Free

< 1 pm

Employment

Social life

Rel - family

90 80 70 60 50 40 30 20 10 0

TLE

Future plans

were found. These related to verbal IQ, full scale IQ, scores on the digit span task and the graded naming test. In all cases, the left temporal group scored significantly lower than the right temporal group. There were no significant differences between the groups on measures of psychological and emotional functioning. We compared the results of the impact scale for the whole group with previous studies examining patients with less severe epilepsy as defined by the frequency of their seizures 1 . Our patients (labelled TLE on Fig. 1) were more likely to report a greater impact than patients with less frequent seizures (see Fig. 1).

Fig. 1: Percentage of patients who reported that an individual domain on the impact of epilepsy scale was a significant problem.

DISCUSSION Our sample of people with intractable TLE showed some degree of both emotional and neuropsychological deficit on the measures administered. Although they reported no depressive symptoms, there was evidence for mild levels of anxiety, as measured by the hospital anxiety and depression scale. Anxiety has been cited as being one of the most common consequences of the unpredictable nature of some epilepsies and often contributes to withdrawal from social situations and reduction in activities 31 . A number of studies investigating the incidence of anxiety in people with resistant epilepsy using the HADS have reported rates of between 25–33 percent 8, 9 . Anxiety can present as part of the individual’s personality (trait) or as part of the epilepsy itself (pre-ictal, ictal, post-ictal phenomena). Rates of depression (utilising the HADS) in an epilepsy population ranged between 10–15 percent 8, 9 . Compared to rates in the general population, suicide is four to five times more common in people with epilepsy and 25 times more common in TLE 32 . In clinical practice, therefore, it is important that symptoms of depression and suicidal ideation are addressed. In contrast to the findings of other researchers, who reported a higher incidence of depression in left, compared to right hemisphere damaged individuals, we found no evidence to support this theory of emotional lateralisation 33, 34 . However,

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Table 4: Results of ANOVAs performed on psychometric variables across two temporal groups (LTL = left temporal lobe; RTL = right temporal lobe). Variable

LTL (n = 109) Mean SD

RTL (n = 84) Mean SD

F-value

Significance

Age

31.08

9.9

31.51

9.73

0.091

0.763

Years of education

11.67

1.66

12.04

2.42

1.546

0.215

Onset of epilepsy

11.76

10.33

13.10

8.08

0.928

0.337

9.64 6.52

4.25 3.41

11.72 6.94

5.23 4.92

2.380 0.134

0.129 0.716

Impact of Epilepsy

27.38

6.90

28.00

8.41

0.031

0.862

WAIS-R: Verbal IQ Performance IQ Full scale IQ

88.08 87.41 86.91

13.51 13.29 12.76

92.91 91.11 91.23

13.55 14.34 13.38

5.847 3.292 5.065

0.017∗ 0.071 0.026∗

NART-R: Verbal IQ Performance IQ Full scale IQ

96.94 98.12 97.39

13.38 12.63 14.11

100.27 100.84 100.65

11.00 10.27 11.21

2.999 2.258 2.630

0.085 0.135 0.107

WMS-R: Verbal memory Visual memory General memory Attention/conc.n Delayed recall

78.41 94.48 79.79 84.67 79.98

15.35 20.50 18.42 19.95 19.15

81.89 92.75 82.88 90.12 82.88

15.77 19.74 17.82 20.05 19.19

2.378 0.348 1.375 3.524 1.073

0.125 0.556 0.242 0.062 0.302

Subtests: Mental control Logical memory I Visual PA I Verbal PA I Visual reproduction I Digit span Visual memory span Logical memory II Visual PA II Verbal PA II Visual reproduction II

5.00 16.78 11.34 14.56 33.35 12.98 14.16 11.44 4.48 5.61 26.13

1.31 7.78 4.48 4.74 7.21 4.41 4.32 7.95 1.74 1.95 10.83

5.08 18.28 11.01 15.49 32.40 14.87 14.45 12.61 4.46 6.14 25.45

1.16 7.10 4.15 4.88 7.76 4.65 3.84 7.56 1.81 1.75 10.84

0.209 1.851 0.263 1.723 0.747 7.941 0.230 1.053 0.007 3.749 0.177

0.648 0.175 0.609 0.191 0.389 0.005∗ 0.632 0.306 0.932 0.054∗∗ 0.674

Graded naming

12.71

5.84

15.41

5.04

6.203

0.014∗

Verbal fluency

32.98

13.28

34.83

14.87

0.322

0.572

Stroop percentile

29.78

35.01

34.11

43.19

0.145

0.705

HADS: Anxiety Depression

∗ P< 0.05; ∗∗ P< 0.06. Note: HADS = Hospital anxiety and depression scale; WAIS-R = Wechsler adult intelligence scale-revised; NART-R

= National adult reading test-revised; WMS-R = Wechsler memory scale-revised; PA = Paired associates.

one of the limitations of this study is that we did not document what proportion of patients were receiving pharmacological treatment for depression. Although this was not addressed in our study, some researchers have reported a clear relationship between the level of seizure activity and psychological functioning; Jacoby and colleagues 1 , investigating a community sample, found that individuals with more frequent seizures showed higher rates of both anxiety and depression. Our sample consisted of patients with high seizure frequency intractable epilepsy being assessed for elective resective surgery and hence it was surprising that such a low level of emotional distress was reported. Participants did report significant

adverse effects of their epilepsy and treatment influencing their day-to-day functioning, suggesting that, despite frequent and disabling seizures, some people felt able to cope with these adverse consequences without a concomitant rise in anxiety or depression. It must be noted, however, that the range of scores on the HAD scale extended up into the severe range, although this was only for a small number of people. Neuropsychological functioning, the ability to retain, assimilate and act effectively on environmental information is an essential requirement for day-today functioning. Impairment in neuropsychological functioning has significant consequences for an individual’s ability to communicate, maintain social

Temporal lobe epilepsy: neuropsychological and emotional consequences

relations, work, play and retain their self-esteem. Clinical anecdotal evidence suggests that individuals with such deficits may be more prone to depression and anxiety, although there clearly exists a reciprocal relationship. According to Trimble 35 , orientation places neuropsychological functioning as central to quality of life. Our results indicate that people with chronic epilepsy tend to have reduced intellectual abilities compared to expected levels predicted by their current reading ability. As a group they show average performance on memory for visual material, but poorer ability when remembering verbal information. Expressive language skills, important in everyday life for communication and social functioning, are impaired in our epilepsy sample. This is likely to have a significant effect on their ability to interact effectively in society and to adequately express themselves and their needs to others. Our results indicate that people with resistant LTL seizures are more likely to suffer greater neuropsychological difficulties than those with right temporal lobe seizures. In line with the lateralisation hypothesis, verbal intelligence, verbal memory and expressive language abilities were reduced in the left temporal group compared to the right temporal group. Interestingly, general intellectual ability was also lower in left temporal individuals. Our results support those of Goldstein and Polkey 22 , who identified a tendency towards lower verbal IQ in left temporal individuals but also a lower performance IQ in right temporal groups. Learning and memory deficits are the earliest and most frequently cited cognitive alterations in patients with TLE 36 . In support of our findings, some researchers have reported patients with left TLE to be impaired on verbal memory tasks 10, 37, 38 . Contrary to our finding of language impairment in left temporal groups, Hamberger and Tammy 39 found no difference in scores on a visual naming task for left and right temporal groups, but other researchers report results in line with our findings 11, 40 . Given the findings of our study that people with epilepsy are susceptible to changes in their intellectual and memory functioning, some consideration should be given to strategies for remediation of these effects. Unfortunately there is very little documented in the literature concerning the neuropsychological rehabilitation of patients with intractable epilepsy, and to date there have been no randomised studies documenting any benefits from such an intervention. In our own unit we have enrolled patients in outpatient memory classes but without systematically evaluating the effectiveness of such a programme. Aldenkamp and colleagues 41 have recently addressed this area and suggest that compensatory memory strategies (the use of internal and external memory aids) are more effective than a reconstruction

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approach (utilising systematic practice techniques). Clearly, this is an area worthy of further investigation. In a series of group training sessions the authors reported small but significant improvements in memory functioning which led to an increase in participants’ independence 42 . Reviewing the psychological interventions for patients with intractable epilepsy is beyond the scope of this paper. Nevertheless there have been a number of studies that have addressed the benefits of psychological intervention. Effective treatments have included anxiety management and relaxation, individual counselling and education, cognitive behavioural therapy and in some cases family therapy may be indicated 43 . There is no doubt that patients with intractable epilepsy would benefit from such interventions, and as such, these should be made routinely available as part of the overall management plan. This study clearly highlights that the management of intractable epilepsy should go beyond initiatives to reduce the frequency of seizures. The authors strongly recommend that attention should also be paid to the psychological and neuropsychological consequences of the condition which may for some patients be as disabling as the seizures themselves.

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