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Special issue: Note

Accelerated long-term forgetting after TIA or minor

stroke: A more sensitive measure for detecting
subtle memory dysfunction?

Sofie Geurts a,*, Sieberen P. van der Werf b,c,d, Vincent I.H. Kwa e and
Roy P.C. Kessels f,g
a
Canisius Wilhelmina Hospital, Department of Medical Psychology, Nijmegen, The Netherlands
b
University of Amsterdam, Department of Psychology, Brain and Cognition, Amsterdam, The Netherlands
c
OLVG, Department of Psychiatry and Medical Psychology, Amsterdam, The Netherlands
d
Rijnstate Hospital, Department of Medical Psychology, Arnhem, The Netherlands
e
OLVG, Department of Neurology, Amsterdam, The Netherlands
f
Radboud University, Donders Institute for Brain, Cognition and Behaviour, Nijmegen, The Netherlands
g
Radboud University Medical Center, Department of Medical Psychology, Nijmegen, The Netherlands

article info abstract

Article history: Cognitive changes after minor stroke or TIA have been reported, with studies describing a
Received 30 March 2017 ‘vascular’ cognitive profile with spared episodic memory. Still, many patients also report
Reviewed 28 September 2017 memory complaints. Studies using long-term forgetting paradigms have detected memory
Revised 4 December 2017 impairment after prolonged intervals in contrast to standard delayed testing in other pa-
Accepted 3 April 2018 tient groups. This study examined whether accelerated long-term forgetting (ALF) is pre-
Published online xxx sent in patients with minor stroke or TIA by comparing one-week delayed recall and
recognition with the performance of a healthy control group. Results revealed that the
Keywords: patients' performance after one week was worse than the controls, in the absence of an
Long-term memory impairment after a short delay. Patients did, however, not report more memory worries
Episodic memory than controls. Possibly, reduced effort, attention or mnemonic strategies may contribute to
Stroke subtle consolidation problems, which go undetected in daily functioning.
Transient ischemic attack © 2018 Elsevier Ltd. All rights reserved.
Vascular cognitive impairment

otherwise good prognosis (Fens et al., 2013). For instance, six

1. Introduction months after minor stroke Dassonville et al. (2016) found high
levels of cognitive complaints and objective cognitive im-
Studies addressing the cognitive consequences after transient
pairments in the domains of memory, executive functioning
ischemic attack (TIA) and minor stroke are scarce, although
and processing speed. Also, Van Rooij et al. (2014) reported
many patients experience cognitive changes despite the

* Corresponding author. Canisius Wilhelmina Hospital, Department of Medical Psychology, Weg door Jonkerbos 100, 6500 GS, Nijmegen,
The Netherlands.
E-mail address: s.geurts@cwz.nl (S. Geurts).
https://doi.org/10.1016/j.cortex.2018.04.002
0010-9452/© 2018 Elsevier Ltd. All rights reserved.

Please cite this article in press as: Geurts, S., et al., Accelerated long-term forgetting after TIA or minor stroke: A more sensitive measure
for detecting subtle memory dysfunction? Cortex (2018), https://doi.org/10.1016/j.cortex.2018.04.002
2 c o r t e x x x x ( 2 0 1 8 ) 1 e7

cognitive impairments after TIA in over a third of their patient

group, the most affected domains being working memory,
2. Method
processing speed and attention, whereas episodic memory
2.1. Participants
was spared. A comparable cognitive profile was found by
Mandzia et al. (2016), p. 90 days after the minor stroke or TIA
We included 30 patients (17 men) who had either experienced
episodic memory performances were within the normal
a TIA or a minor stroke, .5e6 months prior to the assessment.
range, but a lower performance in the of domains attention
The diagnosis of minor stroke or TIA was made by a neurol-
and executive functioning was demonstrated.
ogist in accordance with established criteria (NINDS, 1990).
This ‘vascular’ cognitive profile of attention and executive
The modified Ranking Score (mRS) was used to measure
dysfunction with spared episodic memory function has been
disability in daily activities of the patient group (Sulter, Steen,
related to subcortical brain damage (Zamboni et al., 2017; Van
& de Keyser, 1990). The vast majority of the patient group (27/
Rooij et al., 2017). However, considering the high levels of re-
30) was tested one to three months post-stroke. Other inclu-
ported memory complaints (Dassonville et al., 2016; Fens
sion criteria were that the age- and education-adjusted per-
et al., 2013), the spared episodic memory may also result
formance on the Dutch version of the Rey Auditory Verbal
from the insensitivity of memory tests in detecting subtle
Memory Test (RAVLT; Van der Elst, van Boxtel, van Breukelen,
decrements. Several studies have indeed found that patients
& Jolles, 2005) had to be within the normal range (defined as an
with near-normal performances on standard 30-min delayed-
age- and education-adjusted T-score >35 for the total number
recall tests displayed accelerated long-term forgetting (ALF)
of words recalled in the five learning trials and for the delayed
after a prolonged delay (i.e., days to weeks) (Butler & Zeman,
recall test for which excellent norms are available) and that
2008).
the participant's age was below 75.
ALF has been consistently shown in patients with temporal
Patients were mainly included via a larger study in which
lobe epilepsy (TLE) (Muhlert et al., 2011). Butler et al. (2007)
TIA and minor stroke patients were followed-up after the
compared the performance on the Rey Auditory Verbal
event to monitor changes in cognition, psychological burden
Learning Test (RAVLT) of 50 patients with transient epileptic
and quality of life. This larger cohort existed of 375 patients, 35
amnesia to that of 24 healthy controls after 30-min, one-week
of whom completed the full RAVLT protocol required for this
and three-week delays. After one week, the patients showed a
study. One more patient was included after a regular referral
considerably larger decline on the RAVLT recall scores
for neuropsychological assessment because of concerns about
compared to the controls. In addition to ALF for words and
her cognitive functioning. The diagnosis of minor stroke of
procedural skills, Muhlert, Milton, Butler, Kapur, and Zeman
this one patient was based on the same NINDS criteria as was
(2010) demonstrated faster forgetting of everyday events in
for the other patients. All 36 patients fulfilled the inclusion
patients with transient epileptic amnesia over a period of
criteria of the normal range of T-scores on the RAVLT, but 6
three weeks in comparison to controls. These findings were
patients had to be excluded based on their age (
75), leading
subsequently replicated in TLE patients using intervals up to 8
to the remaining group of 30. All patients were living inde-
weeks (see Elliot, Isaac, & Muhlert, 2014, for a review). Two
pendently at home. The Hospital Anxiety and Depression
possible accounts regarding the underlying mechanisms of
Scale (HADS) was used to screen for signs of major mood
ALF have been proposed, that is, a disruption of ‘late’ memory
problems, using the following classifications: 0e7 (normal),
consolidation or subtle (and consequently undetected) early
8e11 (mild), 11e14 (moderate) and 14e21 (severe) (Hung, Liu,
acquisition problems (Cassel, Morris, Koutroumanidis, &
Wang, Yao, & Yang, 2012; Snaith, 2003). See Table 1 for the
Kopelman, 2016).
mean HADS outcomes (note that the HADS was not admin-
A recent review focusing on ALF in other patient groups,
istered in two patients); none of the patients were known to
such as Alzheimer's disease, Multiple Sclerosis and traumatic
have been diagnosed with a major depressive disorder. Two
brain injury, however, showed less consistent evidence for
patients reported moderate complaints of anxiety, one patient
ALF (Geurts, van der Werf, & Kessels, 2015). Furthermore, a
reported moderate depressive symptoms and two patients
recent empirical study in patients with mixed etiologies who
reported moderate to severe complaints on both scales.
reported subjective memory complaints demonstrated
In addition, a control group was selected from a database
steeper long-term (i.e., after one week) forgetting in these
with long-term forgetting data of 101 healthy participants.
patients than in controls (Van der Werf, Geurts, & de Werd,
These data had been collected previously; exclusion criteria
2016). However, the heterogeneity of that patient sample
for these participants were a history of a neurologic disorder
limited further conclusions about specific etiologies.
or a current psychiatric disorder. We used this database to
The present study examines long-term forgetting in minor
group-match 28 healthy participants (15 men) on gender, ed-
stroke and TIA patients, also focusing on whether long-term
ucation level and age. For the demographical data and time
forgetting is related to subjective memory complaints in
since event see Table 1. The two groups did not differ with
these patients. We only included patients who performed
respect to age [t (56) ¼ 1.86, p ¼ .07], educational level
unimpaired on regular 30-min delayed recall and recognition
(U ¼ 450.0, Z ¼ .48, p ¼ .63), or gender distribution [c2 (1) ¼ .06,
memory tests. We hypothesized that even after normal
p ¼ .81]. The study protocol for the patients was evaluated and
acquisition the patient group would show enhanced forget-
approved by the local medical ethics committee of the OLVG
ting compared to a matched healthy control group. Further-
in Amsterdam and the Canisius Wilhelmina Hospital in Nij-
more, we expected to find an association between subjective
megen; collection of control data was approved by the
memory complaints and ALF in these patients.

Please cite this article in press as: Geurts, S., et al., Accelerated long-term forgetting after TIA or minor stroke: A more sensitive measure
for detecting subtle memory dysfunction? Cortex (2018), https://doi.org/10.1016/j.cortex.2018.04.002
 c o r t e x x x x ( 2 0 1 8 ) 1 e7 3

Table 1 e Demographic characteristics for all participants, as well as depressive symptoms, anxiety level, stroke details and
cerebrovascular risk factors for the patients.

Patients (N ¼ 30) Controls (N ¼ 28)

Mean (SD) or N Range Mean (SD) Range
Sex distribution (men/women) 17/13 15/13
Age (years) 60.2 (10.5) 28e74 55.6 (8.0) 39e77
Education (level)a 5 2e7 6 1e7
HADS
Anxiety 4.1 (4.8) 0e18
Depression 5.1 (4.2) 0e17
Time since event (days) 67.8 (30.5) 16e182
TIA/minor stroke 4/26
Modified Rankin Scale (mRS)b
0 e No symptoms 3
1 e No significant disability 11
2 e Slight disability 8
3 e Moderate disability 3
First-ever stroke or TIA (yes/no/unknown) 21/1/8
Stroke locationc
Left hemisphere 12
Right hemisphere 8
Bilateral 1
Infratentorial 4
Arteryc
Middle cerebral artery 17
Posterior cerebral artery 2
Vertebrobasilar arterial system 6
Unknown 1
Type 2 diabetes (yes/no) 4/26
Hypertension (yes/no) 16/14
Hypercholesterolemia (yes/no) 6/24
Smoking (yes/no/unknown) 10/19/1

Note:
a
Mode; education level was classified using a 7-point scale based on the Dutch educational system, with ‘1’ reflecting less 6 years of primary
school and ‘7’ university degree. HADS ¼ Hospital Anxiety and Depression Scale: 0e7 (normal), 8e11 (mild), 11e14 (moderate) and 14e21
(severe); note that HADS scores were missing for two patients.
b
mRS was not available for 5 patients.
c
For the minor stroke patients only.

research ethical committee of the faculty of social sciences of
Radboud University in Nijmegen.
2.2. Materials and procedure
The Dutch version of the RAVLT was used to assess verbal
learning, recall and recognition performances. This version of
the RAVLT consists of a list of fifteen non-associated words
that is presented orally over five trials. The total learning score
is the sum of these five trials, with a possible score ranging
from 0 to 75. The standard testing procedure involves a 30-min
delayed-recall test (score range: 0e15), followed by a delayed
recognition test. In the recognition test, the 15 target words
were presented among 15 distracters (scoring range: 0e30, i.e.,
hits þ correct rejections).
In addition to the standard protocol, we added a long-term
delayed recall and recognition test. In the long-term delayed
recognition condition, the original 15 distracters were
replaced with 15 alternative distracters that were chosen from
a parallel RAVLT version (with matching word frequencies for
the distractor items). After one week, all patients were asked
to come back to discuss the results; during that visit the
additional recall and recognition tests were administered. The
controls underwent memory testing with the RAVLT and
completed the Multifactorial Memory Questionnaire (MMQ). It
was agreed upon that they would be contacted by telephone to
provide feedback about their baseline results. After one week
the same testing procedure was followed as described for the
patients. At baseline neither the patients nor the controls
were informed about the one-week follow-up assessment of
the word list.
The MMQ was used to assess subjective memory func-
tioning. In this study, we used two of its three subscales, that
is, MMQ Contentment, reflecting the degree of concern and
contentment regarding memory functioning (18 items, score
range 0e72) and MMQ Ability, assessing daily forgetfulness (20
items, score range 0e80). The MMQ Contentment and Ability
subscales are positively defined, with lower scores indicating
less memory contentment and reflecting more daily forget-
fulness (Troyer & Rich, 2000; Van der Werf & Vos, 2011).
2.3. Data analysis
First, we examined whether the groups differed on the RAVLT
standard outcome measures (i.e., total number of words
recalled during the 5 learning trials, the 30-min delayed recall

Please cite this article in press as: Geurts, S., et al., Accelerated long-term forgetting after TIA or minor stroke: A more sensitive measure
for detecting subtle memory dysfunction? Cortex (2018), https://doi.org/10.1016/j.cortex.2018.04.002
4 c o r t e x x x x ( 2 0 1 8 ) 1 e7
performance and the 30-min delayed recognition) using Stu-
dent's t-tests. Subsequently, we performed a mixed-design
GLM analysis using the recall scores of the RAVLT as within-
subject factor (three levels: trial 5, 30-min and 1-week recall)
and group (patients vs controls) as between-subject factor.
Next, we performed a mixed-design GLM analysis on the
recognition data (two levels: 30-min and 1-week recognition),
again with group (patient vs controls) as between-subject
factor. The assumption of normality of the data was exam-
ined using the skewness and kurtosis statistics for all vari-
ables and Mauchly's W was computed to examine the
sphericity assumption.
Using the two delayed recall scores (i.e., after 30 min and
one week) we calculated the percentage of information loss
(Recall Decline) as follows: [100  (standard 30-min recall
score e one-week recall score)/standard 30-min recall score].
The same formula was used with the delayed recognition
scores for the percentages of information loss on the recog-
nition condition (Recognition Decline). The Recall and Recog-
nition Decline scores as well as the MMQ scores were
compared across the groups using Student's t-tests. Effect
sizes were computed (h2p for the GLM factors and Cohen's d for
t-tests). Pearson correlation coefficients (r) were computed for
the patients and controls separately to examine the associa-
tions between the Recall and Recognition Decline measures,
the MMQ subscales, and the time post-event.
3. Results
Skewness and kurtosis statistics showed all variables were
normally distributed. The two groups did not differ signifi-
cantly with respect to the total score on the five learning trails
[Mcontrol ¼ 47.9, SD ¼ 7.4; Mpatients ¼ 47.2, SD ¼ 9.5; t (56) ¼ .31,
p ¼ .76], the 30-min delayed recall score [t (56) ¼ .165, p ¼ .87,
see Fig. 1] and the 30-min delayed recognition score
[t (56) ¼ .953, p ¼ .35, see Table 2] of the RAVLT.
Fig. 1 shows the RAVLT free recall scores immediately after
trial 5, the 30-min delay and after 1-week. For the GLM
Fig. 1 e Mean number of words recalled (þS.E.M.) on the
RAVLT after immediate testing (i.e., after trial 5), a 30-min
delay and a one-week delay for the TIA and minor stroke
patients and the healthy controls (max. ¼ 15); *p < .05.
Please cite this article in press as: Geurts, S., et al., Accelerated long-term forgetting after TIA or minor stroke: A more sensitive measure
for detecting subtle memory dysfunction? Cortex (2018), https://doi.org/10.1016/j.cortex.2018.04.002
analysis on the free-recall scores, the sphericity assumption
was violated [W ¼ .658, c2 (2) ¼ 23.0, p < .0005], so Greenhouse-
Geisser corrections were applied. The results showed a sig-
nificant main effect of Time [F (1.49, 83.5) ¼ 142.1, p < .0005,
h2p ¼ .717], a Time  Group interaction [F (1.49, 83.46) ¼ 5.3,
p ¼ .013, h2p ¼ .086], but no main effect of Group [F (1,56) ¼ 1.4,
p ¼ .291, h2p ¼ .020]. Follow-up t-tests showed that while the
free recall performance did not differ between the two groups
after 30 min (see above, d ¼ .04), the patients showed
a worse free-recall compared to the controls after 1 week
[t (56) ¼ 2.318, p < .024; d ¼ .61]. With respect to the recog-
nition performance (see Table 2), the GLM analysis showed a
significant main effect of Time [F (1, 56) ¼ 63.9, p < .0005,
h2p ¼ .533], but neither a main effect of Group [F (1, 56) ¼ 1.0,
p ¼ .334, h2p ¼ .017] nor a Time  Group interaction
[F (1, 56) ¼ .3, p ¼ .606, h2p ¼ .005].
For the decline scores (see Table 2), a significant group
difference was found on Recall Decline [t (56) ¼ 3.286, p < .002]
but not on Recognition Decline [t (56) ¼ .614, p ¼ .542], indi-
cating that the percentage of information loss after one week
was significantly higher for the patients than the controls on
the recall measures but not on the recognition scores.
With respect to the MMQ (see Table 2), three patients did
not fully complete the questionnaire. MMQ analyses were
performed with the remaining 27 patients and all controls. No
significant differences were found between patients and
controls on MMQ Ability [t (53) ¼ .974, p ¼ .34] or MMQ
Contentment [t (56) ¼ 1.221, p ¼ .23]. A significant positive
correlation was found in the patient group between the MMQ
Ability score and Recognition Decline (r ¼ .39, p ¼ .04). Higher
subjective memory ability scores were associated with more
long-term recognition decline. A significant negative correla-
tion was found in the control group between the MMQ
Contentment score and Recall Decline (r ¼ .39, p ¼ .04). In
this group higher memory contentment scores were associ-
ated with less decline on long-term recall. Time after stroke or
TIA was not significantly correlated with Recall Decline
(r ¼ .317) or Recognition Decline (r ¼ .247).
4. Discussion
In this study we investigated whether abnormal long-term
forgetting occurs in patients with minor stroke or TIA, who
performed in the normal range on standard memory testing.
Results revealed indeed more long-term forgetting in the TIA
and minor stroke patients in comparison to a healthy control
group on free recall. The one-week recognition performance,
however, did not differ between the groups, in line with pre-
vious findings (see Geurts et al., 2015).
Cued recall (as in recognition tests) demands less cognitive
effort, less attention and less mnemonic strategies in com-
parison to free recall, making recognition tests typically less
sensitive to subtle changes (Reas & Brewer, 2013). It could be
hypothesized that in the case of subtle memory impairment
effort, attention and mnemonic strategies do not affect the
performance after 30 min, but have an increasing effect when
more time has passed, possibly resulting in a sharper decline
of long-term recall abilities as compared to long-term recog-
nition. Furthermore, recognition is thought to rely on two
 c o r t e x x x x ( 2 0 1 8 ) 1 e7
Table 2 e Results for RAVLT delayed recognition and long-term decline as well as MMQ scores.
Patients (N ¼ 30)
Mean (SD) Range
RAVLT Delayed Recognition
Recognition 30 min 29.1 (.9) 27e30
Recognition 1 week 26.7 (2.9) 19e30
RAVLT decline scores (% long-term decline; 1-week vs 30-min)
Free recall 60.4 (28.9) 0e100
Recognition 8.4 (8.5) 3.45e34.5
MMQ (N ¼ 27)
Ability 60.7 (10.7) 35e78
Contentment 54.3 (12.2) 31e72
RAVLT ¼ Rey Auditory Verbal Learning Test (Dutch version); MMQ ¼ Multifactorial Memory Questionnaire; *p < .05.
distinct processes, that is, familiarity (a sense of having seen
an item before) and recollection (remembering that a partic-
ular item have been previously seen, as well as the context in
which it appeared) (Merkowa, Burke, & Kahanac, 2015). These
processes combined may also have facilitated the recognition
performance after 1 week, resulting in a performance similar
to controls in the patients. Alternatively, this discrepancy may
also be the result of a retrieval deficits due to subtle executive
impairments (Unsworth, 2015; Davidson, Troyer, &
Moscovitch, 2005).
Furthermore, we investigated the association between
subjective memory complaints and the actual memory per-
formance. The results demonstrated comparable levels of
memory contentment and complaints of forgetfulness in the
patient group compared to the controls. In addition, the as-
sociations between subjective memory functioning and the
memory performances were in general low. However, the two
significant correlations are interesting. That is, patients who
reported less memory complaints demonstrated more forget-
ting over time on the recognition task. In contrast, healthy
participants who were more content with their memory per-
formance showed less recall decline over time. This suggests
that healthy controls may be better at rating their own
memory functioning in comparison to the patients. Only a few
previous studies have addressed subjective cognitive func-
tioning in minor stroke and TIA. Two studies reported the
presence of memory complaints after minor stroke or TIA
(Dassonville et al., 2016; Fens et al., 2013), while one study
reported that TIA patients did not experience cognitive com-
plaints (Van Rooij et al., 2014). In (major) stroke, subjective
cognitive functioning has been studied more extensively, but
conflicting results on the association between subjective
memory complaints and performances on memory tests have
been found (e.g., Van Rijsbergen, Mark, de Kort, & Sitskoorn,
2014). A lack of insight or emotional distress are possible
causes. An alternative explanation for this discrepancy is that
the subtle memory decline after one week may not have
resulted in noticeable daily problems in our sample, especially
given the relatively short time since the vascular event for
most of the patients. Both assumptions could contribute to the
lack of concordance in this study and even explain why pa-
tients who reported less complaints showed more long-term
forgetting on recognition.
Please cite this article in press as: Geurts, S., et al., Accelerated long-term forgetting after TIA or minor stroke: A more sensitive measure
for detecting subtle memory dysfunction? Cortex (2018), https://doi.org/10.1016/j.cortex.2018.04.002
5
Controls (N ¼ 28) Effect size (Cohen's d)
Mean (SD) Range
29.3 (1.1) 27e30 .20
27.2 (2.0) 23e30 .20
30.8 (39.3) 116.7e81.8 .86*
7.2 (6.2) 3.7e20 .16
58.2 (8.4) 42e75 .26
50.5 (10.9) 28e71 .33
There are some limitations that should be addressed. First,
we analyzed the minor stroke and TIA patients together, as the
sample size was too small to perform subgroup analyses.
Future studies should include a larger group so that TIA and
minor stroke patients can be analyzed separately, to investigate
to what extent each diagnosis contributes to long-term forget-
ting. Also, we only included patients below 75 years of age, as a
result of which the ALF cannot be generalized to minor stroke at
older age. Future studies should also investigate the clinical
significance of ALF in minor stroke and TIA, for example using a
longitudinal approach, to identify those who are at risk for
further cognitive decline. Furthermore it would be interesting to
relate ALF in patients with TIA or minor stroke to neuroimaging
findings, for instance diffusion-weighted imaging (DWI), as
DWI abnormalities have been found in minor stroke and TIA
patients (Brazzelli et al., 2014; Kate et al., 2015; Schulz, Briley,
Meagher, Molyneux, & Rothwell, 2003; Van Rooij et al., 2017).
In sum, this study is the first to investigate long-term
forgetting after cerebrovascular disease, showing that accel-
erated forgetting may be a more sensitive measure in detecting
memory difficulties after minor stroke and TIA than traditional
memory assessment. Based on our results, the delay interval in
memory testing in clinical practice (typically between 15 and
30 min) may be too short. This is also in agreement with
neurobiological findings on episodic memory formation. That
is, there is evidence that consolidation takes place over days
and weeks rather than minutes, possibly mediated by sleep
(Chambers, 2017; Dudai, Karni, & Born, 2015). For instance, ALF
for context location was found in thalamic stroke patients after
24 h, despite normal context memory performances after one
hour (Tu, Miller, Piguet, & Hornberger, 2014).
Future neuroimaging studies combined with more exten-
sive cognitive testing (also including measures of executive
function and mental effort) may provide further insights into
the underlying mechanisms of ALF in TIA and minor stroke
patients.
Acknowledgements
The authors would like to thank the BAC team consisting of
I. Bekker, J. Kramer, and B. Notz for their assistance in the data
collection.
6 c o r t e x x x x ( 2 0 1 8 ) 1 e7

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Please cite this article in press as: Geurts, S., et al., Accelerated long-term forgetting after TIA or minor stroke: A more sensitive measure
for detecting subtle memory dysfunction? Cortex (2018), https://doi.org/10.1016/j.cortex.2018.04.002