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Epilepsy & Behavior 51 (2015) 48–52

Contents lists available at ScienceDirect

Epilepsy & Behavior

journal homepage: www.elsevier.com/locate/yebeh

Subjective cognitive complaints versus objective neuropsychological


performance in older adults with epilepsy
Rachel Galioto a,⁎, Andrew S. Blum b, Geoffrey Tremont a,b
a
Warren Alpert Medical School of Brown University, Providence, RI 02903, USA
b
Rhode Island Hospital, Providence, RI 02903, USA

a r t i c l e i n f o a b s t r a c t

Article history: Memory complaints are common among older adults with epilepsy (OAE), though discrepancy between
Received 28 May 2015 subjective complaints and objective performance often exists. This study examined how accurately OAE and
Revised 16 June 2015 their informants reported on the participant's cognitive difficulties by comparing ratings of everyday cognition
Accepted 18 June 2015
to objective performance. Thirty-seven OAE and 27 older adult controls completed a brief battery of neuropsy-
Available online xxxx
chological tests, the Beck Depression Inventory, and the Cognitive Difficulties Scale (CDS). Each participant had
Keywords:
an informant who completed the CDS. Older adults with epilepsy performed worse than controls on cognitive
Epilepsy testing and reported more subjective cognitive complaints. Neither participant- nor informant-reported
Elderly cognitive complaints were related to performance on any of the neuropsychological tests for either the group
Depression with epilepsy or control group, but both were related to greater depressive symptoms. Results suggest that
Caregiver issues subjective report of cognitive problems by both OAE and their informants may not reliably reflect the extent to
Learning and memory which these problems exist.
© 2015 Elsevier Inc. All rights reserved.

1. Introduction Subjective cognitive complaints are very common among individ-


uals with epilepsy of all ages [9] and are a significant predictor of poorer
Subjective cognitive complaints are common among older adults self-reported quality of life in this group [10]. However, the degree of
and may predict cognitive decline. For example, a recent study among subjective complaints is not consistently associated with objective
cognitively intact older adults demonstrated that subjective memory cognitive dysfunction [11]. Factors such as older age and higher intelli-
complaints were associated with increased risk of cognitive impairment gence level have been associated with greater memory complaints [9]
and Alzheimer-type brain pathology [1]. Subjective cognitive com- while epilepsy characteristics (e.g., seizure type, frequency, AEDs) are
plaints may be particularly prevalent among older adults with epilepsy not consistently related to subjective memory complaints among
(OAE) given that this group demonstrates objective cognitive deficits these individuals [9,12]. Depression, which is very common among pa-
and is at risk for cognitive impairment, particularly for memory tests, tients with epilepsy [13,14], has been consistently shown to be related
compared to older adults without epilepsy [2–5]. In fact, these to both subjective cognitive complaints [10,13,15–19] and objective
individuals have been shown to have similar memory deficits and great- cognitive function [20] in this group. In fact, numerous studies in
er deficits in overall cognition and executive function when compared patients with epilepsy demonstrate a stronger association between
to individuals with Mild Cognitive Impairment [2]. One major contribu- subjective cognitive complaints and mood than between subjective
tor to cognitive deficits in OAE is the use of antiepileptic drugs (AEDs), and objective cognitive functions [15,19,21]. Additionally, reduced
with AED polytherapy associated with the most severe cognitive deficits awareness of cognitive deficits among patients with epilepsy may con-
[2–4]. Seizure characteristics such as age of onset [6], epilepsy duration tribute to an underreporting of deficits and partially account for the dis-
[7], and seizure frequency [8] may also contribute to cognitive dysfunc- crepancy between objective and subjective cognitive complaints [22].
tion in this population, with earlier onset, longer duration, and greater Given this discrepancy, it seems reasonable to examine whether
seizure frequency commonly showing an association with poorer cogni- proxy measures of cognitive complaints, such as informant reports of
tive functioning; however, these findings are not consistent across the cognitive complaints, could more accurately reflect objective cognitive
literature. performance. Informant-reported cognitive complaints have been
shown to be correlated to objective cognitive performance in other pop-
⁎ Corresponding author at: Physician's Office Building Suite 430, 110 Lockwood St.,
ulations, such as dementia and MCI, and among cognitively normal
Providence, RI 02903, USA. Tel.: +1 401 444 4500; fax: +1 401 444 6643. adults [23–25]. However, the utility of informant report of cognitive dif-
E-mail address: gtremont@lifespan.org (R. Galioto). ficulties has not yet been examined among older adults with epilepsy.

http://dx.doi.org/10.1016/j.yebeh.2015.06.035
1525-5050/© 2015 Elsevier Inc. All rights reserved.
R. Galioto et al. / Epilepsy & Behavior 51 (2015) 48–52 49

There were three major aims of the present study. First, we sought to there was a greater percentage of females in the control group com-
characterize subjective cognitive complaints among OAE by comparing pared to the group with epilepsy, χ2 (1, N = 64) = 9.98, p b .01.
them to older adult controls without epilepsy and examine the relation- There were no differences between groups for race or education. See
ship between subjective cognitive complaints and other factors, such as Table 1 for full demographic and seizure characteristics.
demographic factors, mood, and seizure characteristics, in this group. Each participant also had one participant-selected informant (n =
We hypothesized that OAE would endorse greater cognitive complaints 64), defined as someone who the participant thought knew them well
than controls and that older age and greater depressive symptoms enough to provide collateral information about their functioning. Most
would be related to greater cognitive complaints. In terms of seizure informants were spouses or significant others (59.7%), followed by
characteristics, no a priori hypotheses were made given the mixed children (15.6%), siblings (11.3%), friends (11.3%), and parents (1.6%).
findings among younger adults with epilepsy. The second aim was to On average, informants were 58.27 years old (SD = 14.42), had
examine the accuracy of self-reported cognitive complaints among 14.91 years of education (SD = 2.98), and knew the participants for
OAE by comparing subjective cognitive complaints to objective perfor- 34.26 years (SD = 18.75).
mance on neuropsychological tests. As above, a priori hypotheses
were not made as previous research on the relationship between sub- 2.2. Procedure
jective cognitive complaints and objective cognitive function among
younger patients with epilepsy has been mixed. The third aim of this Interested participants were contacted via telephone. After
study was to examine whether informants of OAE could more accurate- obtaining informed consent, interested participants underwent an in-
ly report on the patient's cognitive deficits. It was hypothesized that office neuropsychological testing and completed a number of question-
informants of OAE would be able to more accurately report cognitive naires. Informants accompanied the participants to the evaluation and
difficulties than the patients themselves given previous research in completed questionnaires while participants completed neuropsycho-
other samples which has shown this pattern. logical testing. Participants were compensated for their time after
completion of the assessment. All procedures were approved by the
2. Materials and methods local Institutional Review Board.

2.1. Participants 2.3. Measures

Participants were 37 OAE and 27 older adult controls without 2.3.1. Objective cognitive function
epilepsy. Older adults with epilepsy were recruited through a Participants completed a battery of well-established neuropsycho-
hospital-based neurology practice. Controls were recruited through logical tests. The tests administered and variables used in analyses
community advertising. To be eligible for inclusion, participants were included: Trail Making Test [26] A (TMT-A) and B (TMT-B) time to com-
above the age of 55 years and spoke English as their first language. pletion, Controlled Oral Word Fluency Association Test [27] (COWAT)
Diagnosis of epilepsy was determined by a neurologist and required ob- total correct words, Boston Naming Test [28] (BNT) total correct
jective evidence of seizures (i.e., EEG). Exclusion criteria for both groups words, Animal Fluency total correct words, Rey Complex Figure Test
included a history of mental retardation or other serious developmental [29] (RCFT) copy presence and accuracy score from the Boston Qualita-
disorder, other medical illnesses that affect cognition or are terminal, tive Scoring System, Hopkins Verbal Learning Test [30] total recall
and severe psychiatric conditions (e.g., schizophrenia, bipolar disorder, (HVLT-TR) and delayed free recall (HVLT-DR), and the Brief Visuospatial
and active substance abuse disorder). The group with epilepsy was sig- Memory Test-Revised [31] total recall (BVMT-TR) and delayed free re-
nificantly older, t(60.37) = 2.62, p = .01, than the control group, and call (BVMT-DR).

2.3.2. Subjective cognitive complaints


Table 1
Demographic and epilepsy characteristics, CDS scores, and BDI-II of the sample. The Cognitive Difficulties Scale [32] (CDS) is a self-report measure
given to both patients and informants consisting of 38 items and
Epilepsy (n = 37) Control (n = 27)
assesses cognitive difficulties in daily activities over the past week
Mean (SD)/%/[range] Mean (SD)/%/[range] p (e.g., remembering names, phone numbers, driving directions, names
Age 65.22 (8.10) [55–86] 60.93 (4.95) [55–74] .011 of objects, appointments, running errands, maintaining focus on a
Female 51.4% 88.9% .002 task, losing items, using scissors, fastening clothes, or making mistakes
Education 14.54 (3.19) 15.63 (2.04) .10 in typing). Participants and informants answered these questions on a
Caucasian 100% 92.6% .243
I-CDS 0.85 (0.75) 0.32 (0.36) .001
0–4 scale ranging from never to very often with higher scores reflecting
P-CDS 1.16 (0.71) 0.60 (0.43) .001 greater cognitive complaints. In order to adjust for missing item
BDI-II 10.05 (9.82) 2.22 (2.94) .001 responses, an average score for patient and informant CDS score was
Age first seizure 39.67 (25.14) – – calculated by dividing total score by number of items completed. Partic-
Duration (years) 25.25 (21.38) – –
ipant and informant average CDS scores ranged from 0 to 4.
Monthly Sz (past year) 1.43 (1.85) – –
AEDs 1.76 (0.86) – –
Etiology 2.3.3. Participant depression
Idiopathic 54.1% – – The Beck Depression Inventory-II (BDI-II) [33] was used to assess de-
Trauma 13.5% – – pressive symptoms among participants. Scores range from 0 to 63 with
Neoplasia 8.1% – –
higher scores reflecting greater depressive symptoms. Raw scores were
Infection 8.1% – –
Vascular 8.1% – – used in analyses.
Unknown 8.1% – –
Location 2.4. Statistical analyses
Temporal 48.6% – –
Frontal 10.8% – –
Multifocal 10.8% – – Descriptive statistics were used to examine sample characteristics
Generalized 8.1% – – and differences between groups. Raw scores for the neuropsychological
Unknown 21.6% – – tests were corrected for age, gender, and education when possible,
Note: BDI—Beck Depression Inventory-II, Sz—seizures, AED—number of antiepileptic using well-established normative data, and converted into T-scores
drugs, P—patient, I—informant, CDS—Cognitive Difficulties Scale. (mean of 50, standard deviation of 10) to facilitate interpretation.
50 R. Galioto et al. / Epilepsy & Behavior 51 (2015) 48–52

Independent sample t-tests were conducted to examine differences be- Table 3


tween the group with epilepsy and control group on participant CDS Correlations between CDS scores and cognitive function for the group with epilepsy and
control group.
scores and neuropsychological tests. Bivariate correlations were con-
ducted for each group separately to examine the relationships among Epilepsy (n = 37) Control (n = 27)
participant CDS scores, demographic factors, objective cognitive func- Participant Informant Participant Informant
tion, and participant-reported depressive symptoms. For the group
TMT-A .16 .25 .25 −.20
with epilepsy, the relationship between these measures and seizure TMT-B .08 .11 .40 −.10
characteristics and AEDs was also examined. Paired-sample t-tests COWAT .23 .28 −.18 .10
were used to examine differences between participant- and informant- Animals .08 −.03 −.14 −.39
reported CDS scores for both groups. Finally, bivariate correlations BNT −.02 .08 .06 .10
RCFT −.11 −.19 .14 .01
examined the relationship among informant-reported CDS scores and HVLT-TR −.32 −.30 −.06 −.15
patient-reported depressive symptoms for the group with epilepsy. HVLT-DR .08 −.06 −.04 −.27
In order to control for multiple comparisons, significance was defined BVMT-TR −.24 −.26 .02 −.20
as p b .01. BVMT-DR −.18 −.19 .24 −.09
BDI-II .74⁎⁎ .54⁎ .11 −.01
Participant age .13 −.09 .12 .60⁎
3. Results Participant education −.38± −.13 .06 .29
Age onset −.15 −.16 – –
Duration .22 .16 – –
3.1. Objective cognitive function and patient-reported subjective cognitive Seizures per month −.18 .14 – –
complaints AEDs .22 .20 – –

Abbreviations: TMT—Trail Making Test, RCFT—Rey Complex Figure Test, COWAT—


Independent sample t-tests indicated that OAE performed worse Controlled Oral Word Association Test, BNT—Boston Naming Test, HVLT—Hopkins Verbal
than controls on nearly all cognitive tests including TMT-A, TMT-B, Learning Test, BVMT—Brief Visual Memory Test-Revised, TR—total recall, DR—delayed re-
COWAT, Animal Fluency, HVLT-TR, HVLT-DR, BVMT-TR, and BVMT-DR. call, AEDs—antiepileptic drugs.
⁎⁎ p b .01.
There were no differences between groups for RCFT. For the group ⁎ p b .05.
with epilepsy, clinically significant impairment (T-score N 1.5 SD ±
Trend toward significance (p = .02).
below the mean) was most common on memory tests (BVMT-TR
(51.4%), BVMT-DR (45.9%), HVLT-TR (29.7%), HVLT-DR (27.0%)), psy-
chomotor speed (TMT-A (35.1%)), and visual organization (27.0%,
3.3. Contributors to subjective cognitive complaints
RCFT). Impairment was much less common in the control group and
most prevalent for visual memory (BVMT-TR (14.8%), BVMT-DR
Bivariate correlations examined the relationships among demo-
(11.1%)). See Table 2 for complete description of neuropsychological
graphic factors, depression, and participant-reported subjective cogni-
test scores and impairment in both groups.
tive complaints separately in the group with epilepsy and control
Participant CDS scores of OAE ranged from 0.05 to 3.00 while control
group. In the group with epilepsy, the relationship between subjective
group participant CDS scores ranged from 0.03 to 1.45. Independent
cognitive complaints and seizure characteristics was also examined. In
sample t-tests demonstrated greater participant CDS scores for the
the control group, CDS scores were not significantly correlated with
group with epilepsy (M = 1.62, SD = 0.71) compared to the control
age, education, or depression. Given that the two groups differed in
group ((M = 0.60, SD = 0.43), t(60.19) = 3.91, p b .001).
terms of gender composition, independent sample t-tests were used
to examine gender differences on CDS scores; results were not signifi-
3.2. Associations between patient-reported subjective cognitive complaints cant, t(67) = −0.58, p = .57, indicating that there were no differences
and objective cognitive performance in CDS scores between males and females.
In the group with epilepsy, greater CDS scores were highly related to
Bivariate correlations were conducted separately in each group to greater depressive symptoms (r = .74, p b .001), and there was a trend
examine the relationships between participant CDS scores and perfor- toward significance for fewer years of education (r = −.38, p = .02).
mance on neuropsychological tests. Subjective cognitive complaints Cognitive Difficulties Scale scores were not related to age or any seizure
were not significantly related to performance on neuropsychological characteristics including AEDs, seizures per month in the past year,
tests in either the group with epilepsy or control group. Table 3 presents duration of epilepsy, or age of onset.
full correlations.

Table 2 3.4. Report of cognitive difficulties: relationships with neuropsychological


Performance and impairment on neuropsychological tests for the group with epilepsy and test performance
control group.

Test Epilepsy (n = 37) Control (n = 27) Independent sample t-tests revealed that informants of OAE had sig-
nificantly higher CDS scores than informants of controls, t(55.24) =
Mean (SD) Impaired Mean (SD) Impaired t p
3.74, p b .001. In addition, participants with epilepsy reported greater
TMT-A 37.97 (12.26) 35.1% 48.44 (7.48) 3.7% −4.18 b.001 cognitive difficulties compared to what their informants rated of
TMT-B 43.65 (10.69) 16.2% 52.41 (7.46) 3.7% −3.61 .001
them, t(36) = 3.14, p b .01. This pattern neared significance among
RCFT 47.22 (16.03) 27.0% 51.52 (9.68) 7.4% −1.33 .188
COWAT 43.89 (9.07) 21.6% 55.48 (9.38) 0.0% −4.98 b.001 control participants with the control participants endorsing more
Animals 44.89 (9.71) 16.2% 53.41 (7.47) 0.0% −3.81 b.001 cognitive difficulties than their informants rated of them, t(26) =
BNT 46.84 (14.97) 18.1% 54.89 (4.99) 0.0% −3.05 .004 2.78, p = .01.
HVLT-TR 45.11 (12.13) 29.7% 53.89 (8.09) 0.0% −3.47 .001
For the group with epilepsy, informant report of cognitive difficulties
HVLT-DR 41.27 (15.10) 27.0% 53.96 (7.78) 3.7% −4.38 b.001
BVMT-TR 39.73 (13.84) 51.4% 48.37 (10.33) 14.8% −2.73 .008 was also not related to any of the neuropsychological tests. However,
BVMT-DR 38.57 (16.02) 45.9% 48.30 (14.55) 11.1% −2.49 .015 there was a relationship between informant CDS score and patient-
Note: TMT—Trail Making Test, RCFT—Rey Complex Figure Test, COWAT—Controlled Oral
reported depressive symptoms (r = .54, p b .01). There was also no re-
Word Association Test, BNT—Boston Naming Test, HVLT—Hopkins Verbal Learning Test, lationship between informant CDS scores and neuropsychological tests
BVMT—Brief Visual Memory Test-Revised, TR—total recall, DR—delayed free recall. or depression among the control participants.
R. Galioto et al. / Epilepsy & Behavior 51 (2015) 48–52 51

4. Discussion functioning. This finding is consistent with one study in a sample of


elderly individuals without dementia that found informant report of
The present study sought to characterize and examine the accuracy memory complaints was related to higher patient scores on a self-
of subjective cognitive complaints among OAE; examine the relation- report measure of depression [35]. The authors hypothesized that this
ship between subjective cognitive complaints and demographic factors, relationship may be the result of the informant's misattribution of psy-
mood, and seizure characteristics; and determine whether informants chological problems to memory deficits or that the participant was
of OAE could more accurately report on the patient's cognitive deficits. more likely to discuss their cognitive concerns with the informant due
It was hypothesized that OAE would endorse more cognitive complaints to their psychological state. Regardless, it seems that depression can in-
than controls, that older age and greater depressive symptoms would be fluence informant report of cognitive difficulties and clinicians and re-
related to greater cognitive complaints, and that informants of OAE searchers should be aware of this. Overall, our results suggest that
would be able to more accurately report cognitive difficulties than the informants of OAE may not be able to adequately report on the patients'
patients themselves. cognitive functioning and highlight the need for the identification of ad-
Results of this study demonstrated that, as expected, OAE demon- ditional means of assessing cognitive complaints in OAE that are not as
strated poorer cognitive function and endorsed greater cognitive com- highly influenced by related factors such as mood.
plaints than controls. Consistent with previous research, subjective This study must be viewed in light of a number of limitations. First,
cognitive complaints in the group with epilepsy were related to greater the small sample size and entirely Caucasian sample limit the generaliz-
depressive symptoms and lower education. We did not find a relation- ability of these findings. Second, we found no relationship between sub-
ship between subjective cognitive complaints and seizure characteris- jective cognitive complaints and a number of demographic and
tics which is, perhaps, not surprising given the mixed results observed epilepsy-related factors. This may have been due to small sample size,
in other studies. Importantly, cognitive complaints were not related to a relatively healthy sample, or the heterogeneity of individuals in the
performance on any of the neuropsychological tests for either group. group with epilepsy in terms of seizure characteristics. Future research
This is not entirely surprising for the control group, likely owing to in a sample large enough to examine possible subgroup effects is need-
restricted range of scores both for neuropsychological tests and for the ed to clarify these results. Lastly, the OAE and control groups differed in
CDS. However, the absence of a relationship between subjective their gender composition; however, this was unlikely to contribute
complaints and objective cognitive function in OAE deserves attention. highly to the results as independent sample t-tests demonstrated no
Previous research consistently demonstrates discrepancy between the differences in CDS scores between genders.
degree of cognitive impairment and subjective complaints among indi- Overall, this study demonstrated that although objective cognitive
viduals with epilepsy, though this is the first study to demonstrate this impairment is common among OAE, subjective report of cognitive prob-
discrepancy among older individuals with epilepsy. One possible reason lems by both patients and informants may not reliably reflect the extent
for the discrepancy in this sample is the influence of depression on cog- to which these problems exist, but rather may be a marker for depres-
nitive complaints given the strong relationship between BDI and CDS sive symptoms. Future research is needed to identify alternative
scores in the group with epilepsy. It is difficult to determine the extent means of assessing cognitive complaints in this population.
to which depression is influencing cognitive complaints in this sample
given the small sample size and relatively low levels of depression ob-
Acknowledgments
served. However, the highly significant associations between depressive
symptoms and patient-reported cognitive complaints suggest that
This work was supported by an Intradepartmental Seed Grant from
cognitive complaints may be a proxy for depressive symptoms in this
the Department of Neurology, Alpert Medical School, Brown University.
population. Another possibility is that existing measures of cognitive
complaints, such as the CDS which was used in this study, are not partic-
Conflict of interest
ularly sensitive measures of cognitive difficulties in populations with
epilepsy. Future research is needed to further examine this possibility.
The authors declare no conflicts of interest.
Overall, these results raise significant concern for the utility of self-
report measures of cognition in this population.
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