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CYBERPSYCHOLOGY, BEHAVIOR, AND SOCIAL NETWORKING

Volume 00, Number 00, 2018


ª Mary Ann Liebert, Inc.
DOI: 10.1089/cyber.2017.0679

Cognitive Stimulation of Elderly Individuals with Instrumental


Virtual Reality-Based Activities of Daily Life:
Pre-Post Treatment Study

Pedro Gamito, PhD,1,2 Jorge Oliveira, PhD,1,2 Diogo Morais, MSc,1,2 Cátia Coelho, MSc,3 Nuno Santos, MSc,3
Catarina Alves, BA,3 Ana Galamba, BA,3 Miguel Soeiro, MSc,4 Madhurrima Yerra, BA,5 Hannan French, BA,5
Lily Talmers, BA,5 Tiago Gomes1 and Rodrigo Brito, PhD1,2
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Abstract

As the demographic structure in western societies ages, the prevalence and impact of cognitive decline rises.
Thus, new solutions to tackle this problem are required. The use of Information and Communication Tech-
nologies (ICT)-based cognitive exercises has emerged in the last few decades, though with inconsistent results.
Hence, we conducted a pre-post treatment study to further investigate this approach. We designed a set of
virtual reality exercises that mimic activities of daily living by which the patient can train different cognitive
domains. Twenty-five participants, ages 65–85, underwent 12 training sessions between the pre-treatment and
post-treatment assessments. Significant increases were seen between the two assessments for some of the
neuropsychological measures: visual memory, attention, and cognitive flexibility. Results also suggest that
participants with lower baseline cognitive performance levels improved most after these sessions.

Keywords: cognitive stimulation, virtual reality, serious games, elderly

Introduction tive domain and design choice were the primary factors
behind the efficacy of the specific technique used.6 A set of

A s the population ages in developed countries, namely


in Europe (in 2030 * 25 percent of EU citizens will be
over 65 years old1), new challenges arise from the growing
seven randomized controlled trial studies (RCTs) tested a
variety of techniques to enhance memory, executive rea-
soning, and processing speed; a meta-analysis of its results
burden of age-related conditions and diseases on national showed that cognitive training had some long-lasting effects
health systems and consequent needs to develop better treat- on performance.7
ments for those conditions. The negative impact of aging on In a literature review including 10 RCTs, patients in only
cognitive functioning, which is our focus, is well known.2 half of the trials reviewed showed cognitive improvement,
Studies testing traditional techniques to improve cognitive with no visible long-lasting or crossover effects in domain
functioning have shown some therapeutic success. A sys- functionality; the authors of the review concluded that there
tematic review3 found that cognitive stimulation, particularly was no evidence that structured cognitive interventions are
in dementia patients, promotes gains in cognitive function as effective.8 Another systematic review on cognitive and
well as in both general wellbeing and quality of life (QoL). memory training in adults at risk of dementia highlighted some
Similar results were found in another review.4 promising results but suggested that more RCTs are required
One alternative to traditional strategies and exercises is the to provide robust support for the success of these techniques.9
use of ICT (Information and Communication Technologies) Another review highlighted the significant effect of such
programs. The evidence to support ICT-based solutions to therapies on working memory, with clearer results in patients
overcome age-related cognitive decline is, nevertheless, not with less prior training; furthermore, the results show prom-
yet robust5: modest improvements were found in studies ising effects in the transfer of skills from the training context to
involving computerized cognitive training (CCT). Cogni- everyday living.10 Authors of a review devoted specifically to

1
School of Psychology and Life Sciences, Lusophone University of Humanities and Technologies, Lisbon, Portugal.
2
HEI-Lab: Digital Human-Environment Interaction Lab, Lisbon, Portugal.
3
Junta de Freguesia de Benfica, Gabinete de Psicologia do Pelouro dos Direitos Sociais e Saúde, Lisbon, Portugal.
4
Department of Informatics, Universidade de Lisboa Instituto Superior Tecnico.
5
University of Michigan College of Literature Science and the Arts, Ann Arbor, Michigan, Lisbon, Portugal.

1
2 GAMITO ET AL.

computer-based approaches6 also found interesting results to and 74 (M = 74; standard deviation [SD] = 5.27; ranging from
support these solutions, but they warned against using these 65 to 85 years) were recruited at the center and participated
solutions outside of a broader rehabilitation program super- in this study. Their average education level was 6 years of
vised by specialists. A more positive outlook is presented in a school (SD = 2.42; ranging from 4 to 12 years). Exclusion
review in which the authors conclude that the computerized criteria were as follows: (a) having been clinically diagnosed
training is at least as effective as traditional solutions.11 In that with a psychiatric or neurological disorder and (b) a history
same review, the authors found that most of the issues raised of alcohol or substance abuse. Two participants were ex-
when addressing computer-based solutions are not confirmed cluded because of depression, and one participant, because of
by the results. Furthermore, these solutions were found to transient ischemic attack.
often provide swifter, less labor-intensive, and more effective
alternatives to traditional approaches. Measures
It is now common to find serious games (SG) allied to
The neuropsychological measures used in this study are
virtual reality (VR). SGs have all the properties of their less
all well-established measures with good psychometric
serious cousins. However, these games are designed not for the
properties: the Montreal Cognitive Assessment (MoCA),20
entertainment of players, but to produce a positive impact on
used for cognitive screening; the Frontal Assessment Bat-
the player’s mental and physical health.12 VR/SG apps sim-
tery (FAB),21 a set of six subtests that assess executive
ulate real-life environments. Unlike traditional paper-and-
functioning; the Wisconsin Card Sorting Test (WCST),22
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pencil instruments, these apps provide ecological validity to


commonly used to assess executive functions and cognitive
assessment and stimulation. They also provide behavioral in-
flexibility; the Rey Complex Figure,23 used to assess visuo-
dicators to the therapist by monitoring and recording partici-
constructive abilities and visual memory; and d2,24 used to
pants’ performance during the VR activities.13 Larson et al.
measure attention/concentration. Depression and func-
provide a review of the advantages and disadvantages of ICT-
tionality were assessed with self-report scales: The Beck
based procedures for mental health purposes.14
Depression Inventory II (BDI-II)25 for depressive symp-
A meta-analysis15 was conducted specifically on the use of
toms, and the Everyday Competence Questionnaire26 for
VR as a therapy for adults with brain trauma. The systems
functionality.
ranged in quality, from fully immersive systems to cheap
online games or videogames. In before-after comparisons,
Procedure
improvements in balance emerged in four case studies and
two small RCTs. In between-group comparisons in these This study was carried out between April 2017 and June
RCTs, no differences were seen between VR and traditional 2017. The participants were selected for cognitive stimula-
therapy. While the authors found that the VR applications tion after enrollment in the multi-domain Memória Ativa
improved cognitive function and that participants rated them Senior (MAS) program. The MAS is a project of the Psy-
more positively than traditional techniques, they found no chology Department of the Junta de Freguesia de Benfica (one
difference in success rates between VR-based and traditional of the 24 civil parishes in Lisbon, Portugal). The MAS has
techniques. A more specific review of VR rehabilitation three main activities: (a) informatics—teaching participants
shows, however, very promising results with this approach, basic computer skills and training them to use social net-
with significant clinical improvements in both memory and works to chat with their relatives; (b) cognitive stimulation—
attention outcomes.16 Authors of a review found that these promoting cognitive functioning through training in daily
solutions showed long-term, significantly positive effects on life activities in VR/SG-based scenarios; (c) social skills—
cognitive performance and psychological outcomes, but they teaching participants skills for recognizing and managing
indicated the need for larger samples, quality of life (QoL) emotions, for communication, and for solving problems.
assessment, and longitudinal design.17 These concerns were After their initial neuropsychological assessments (two
also voiced in another review,18 which further pointed out the 1-hour sessions), the participants were familiarized with the
lack of clinical guidelines and standardized treatment proto- desktop VR system (non-immersive) during two 20-minute
cols; these deficiencies, in turn, limit the potential for a broader sessions. The same system used for training was used for the
implementation of these therapies. Most reviews, however, intervention. A desktop system is better for older patients,
agree on the potential for effective use of VR/SG solutions. whose tendency for weaker eyesight leaves them more prone
Moreover, compared to traditional therapies, VR/SG tech- to cybersickness when using head-mounted display (HMD)
niques demonstrate faster and better results for cognitive re- VR headsets. The virtual environments were developed with
habilitation.19 Unity3d. The application was run on a 15.6¢¢ Asus X555L
In the current study, to contribute to the development of a laptop with 2GB Geforce 920M graphic board. One training
structured program for cognitive intervention focusing on the scenario consisted of a maze in which the participants had to
elderly, we explored the effects of a cognitive stimulation find their way to the exit while collecting several items
using VR/SG within a multidomain program that also in- placed throughout the virtual environment. In the other
cludes the promotion of social skills and informatics training scenario, the participants had to navigate a virtual city by
for elderly people. following directions for specific locations. The cognitive
intervention was performed twice a week for a total of twelve
Methods 30-minute sessions. One of two trained psychologists as-
sisted each participant throughout the sessions.
Sample
The cognitive stimulation in the VR environment included
Twenty-five participants (21 women) of the Day Care several daily life activities designed to train cognitive
Centre of the Benfica Parish, Lisbon, between the ages of 65 functions, such as attention tasks (e.g., selecting ingredients
COGNITIVE STIMULATION WITH VR IN THE ELDERLY 3

to bake a cake), working memory tasks (e.g., shopping at a stability in the calculation of a standardized change between
grocery store), auditory memory tasks (e.g., listening to and test scores.28
remembering news on TV), executive functions (e.g., se- Test-retest scores were then calculated for each neu-
lecting the appropriate clothes to wear, arranging shoes in a ropsychological variable to estimate the stability over time of
shoe closet), as shown in Figure 1—from top-left clockwise, each measure used in the calculation of the RCI. This ap-
the bathroom, living room in the apartment, virtual kitchen proach was developed as an alternative to the limitations of
test, shoe closet test, bedroom, outdoor environment, phar- comparisons between subjects and of situations in which
macy, and art gallery test. The level of difficulty for each cases cannot easily be matched with controls in their indi-
type of task was gradually increased throughout the sessions, vidual characteristics.29
so that, for instance, during the first session the participants The resulting Z-score in RCI measures the performance of
had to complete simple tasks, and during the last session they the participant during post-treatment assessment relative to
had to complete more complex tasks (e.g. to buy several items their baseline for each of the measures. Accordingly, a
in the grocery store). The detailed description of the inter- change exceeding Z – 1.96 ( p < 0.05) reflects a reliable
vention protocol is presented in Supplementary Table S1; neuropsychological change between test scores for a 95
Supplementary Data are available online at www.liebertpub percent confidence interval (CI) (2.5 percent in a positive
.com/cyber). direction and 2.5 percent in a negative direction for a two-
tailed test - [a/2 at 95 percent CI]).
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The RCI is given by the following expression25:


Statistical analysis
To uncover significant changes in actual individual out- x2  x1
RC ¼
comes, we calculated Reliable Change Indices (RCIs) indi- Sdiff
vidually for each neuropsychological outcome.27 The RCI
approach standardizes individual changes according to the where x 2 and x 1 are the scores in each neuropsychological
standard error of difference, which accounts for test-retest measure respectively for post- and pre-treatment assessments,

FIG. 1. Screenshots
depicting some of the tasks
used in VR/SG cognitive
stimulation. VR/SG, virtual
reality/serious games.
4 GAMITO ET AL.

where Sdiff reflects the standard error of difference for test pre-treatment assessment to a normative score (i.e., above 15
scores: points) at the time of post-treatment assessment. The dif-
ferences in all the mean scores were tested with a paired
qffiffiffiffiffiffiffiffiffiffiffiffiffi
sample t-test, which showed significant differences between
Sdiff ¼ 2ðSE Þ2 pre-treatment and post-treatment assessments for the number
of perseverative errors of WCST (t[21] = 2.493; p = 0.021),
which accounts for the standard error of measurement (SE): the score in the memory trial of RCF (t[22] = -3.991;
pffiffiffiffiffiffiffiffiffiffiffiffiffi p = 0.001), error percentage (t[16] = 3.463; p = 0.003), and
SE ¼ S1 1  rxx concentration index of d2 (t[16] = -2.926; p = 0.010).

where the S1 is the SD at pre-treatment, whereas rxx repre- Test-retest reliability scores
sents the test-retest reliability.
The RCIs were calculated individually for each neu- Participants in this sample were retested 3 months after
ropsychological measure. On the basis of 1,000 bootstrap their initial tests. The same neuropsychological instruments
samples, the correlations between the RCI and variables such were used in both assessments. These instruments, which are
as age, education and global cognitive ability at pre- well established, have been extensively studied in the geri-
treatment were estimated with 95 percent CIs, a level chosen atric population. Table 1 depicts the test-retest scores (rxx)
for our sample. These scores were below acceptable (<0.50)
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to account for the small sample size.


for some neuropsychological measures. The significant out-
comes had acceptable scores for test-retest reliability ranging
Results from 0.51 (number of P errors of WCST) to 0.80 (score in
Mean change in each neuropsychological domain memory trial of RCF).
for the overall sample
Reliable change index
Means and SDs were calculated for both the pre-treatment
and the post-treatment assessments to provide an under- The RCIs were calculated for the significant outcomes in
standing of the mean change in the overall sample (Table 1). accordance with the statistical approach used to measure
The changes in the mean values for the neuropsychological change.27 The resulting variables in which the better treat-
measures suggested that most of these changes occurred in ment outcomes were given by a decrease in test scores (i.e.,
the expected direction. The mean scores of the screening error percentages) were reverse scored, so that positive
measures (i.e., MoCA and FAB) increased slightly although scores would describe improvements while negative scores
non-significantly between the pre-treatment and post- would describe deteriorations.
treatment assessments, specifically in the FAB, in which the Figure 2 shows an asymmetry in the distribution of pos-
mean total score changed from a clinical score at the time of itive and negative changes across measures, reflecting a

Table 1. Descriptive Statistics and Test-Retest Scores for the Neuropsychological Variables
Pre-treatment Post-treatment
M1 S1 M2 S2 t rxx
MoCA 22.88 3.05 23.00 4.00 -0.244 0.79
FAB 14.68 2.28 15.48 1.27 -1.528 0.33
WCST trials 125.42 7.70 119.83 13.83 1.687 0.36
WCST errors 57.21 20.19 47.00 21.82 1.762 0.18
WCST P errors 32.21 20.15 23.87 13.26 2.493* 0.51
WCST categories 2.96 2.01 3.87 1.76 -1.622 0.35
RCF copy score 28.88 5.42 28.74 5.16 0.763 0.67
RCF copy time 5.71 3.07 5.96 3.50 0.775 0.57
RCF memory score 11.98 5.24 14.98 5.74 -3.991** 0.80
RCF memory time 3.01 1.77 3.35 1.97 -0.609 0.49
d2 targets processed 337.95 77.13 316.70 79.63 1.106 0.18
d2 errors, % 14.57 14.42 4.23 5.20 3.463** 0.60
d2 global performance 286.32 55.72 303.91 66.32 -1.087 0.41
d2 concentration index 86.84 52.74 118.52 23.67 -2.926* 0.57
ECQ 35.20 5.16 33.56 3.35 1.459 0.42
BDI II 10.28 6.31 10.78 8.31 0.048 0.79
M1, mean values at pre-treatment; S1, SD at pre-treatment; M2, mean values at post-treatment; S2, SD at post-treatment; rxx, test-retest
reliability.
*p < 0.05.
**p < 0.01.
BDI-II, Beck Depression Inventory-II; ECQ, Everyday Competence Questionnaire; FAB, Frontal Assessment Battery; MoCA, Montreal
Cognitive Assessment; RCF, Rey complex figure; RCF memory score, Rey complex figure memory trial total score; SD, standard deviation;
WCST, Wisconsin Card Sorting Test (values are percentages, except the number of categories which is the raw score); WCST P errors,
perseverative errors in the WCST in percentage.
COGNITIVE STIMULATION WITH VR IN THE ELDERLY 5

FIG. 2. Percentages of
cases for positive and nega-
tive change (RCI). RCI,
Reliable Change Index.
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higher proportion of positive change across the outcomes of Since the elderly are generally vulnerable to cognitive de-
the study. The proportion of positive and negative changes cline, we tested whether a 3-month cognitive stimulation
that were unlikely to occur by chance at a 95-percent CI is program would help improve cognitive functioning in this
depicted in Table 2. Changes that were positive (Z > 1.96) or population. Participants showed statistically significant im-
negative (Z < 1.96) in more than 2.5 percent (a/2 for two- provements in attention (d2), in visual memory (Rey Com-
tailed predictions) would probably be due to a treatment plex Figure), and on two indicators of cognitive flexibility
effect, because only the extreme outcomes were considered (WCST), as shown by group analysis.
significant changes. Table 2 shows that improvements A control group would have allowed us to discern the effects
(Z > 1.96) were observed in 9 percent of the sample for of confounding variables (e.g., practice effects) on treatment
WCST (perseverative errors), 22 percent for the RCF (score outcomes. Because we lacked a control group, we adopted a
in the memory trial), 12 percent in error percentage, and 13 more conservative statistical approach based on RCI. This
percent in the concentration index of d2. None of the cases approach has been used in a variety of clinical research studies
showed a significant negative change in neuropsychological because of its ability to detect how much each individual has
outcomes. changed between the pre-treatment and post-treatment as-
sessments while controlling for the standard error of difference
Correlates of cognitive performance between test and retest scores.28,29 This change results in a
We also explored whether these improvements were re- standardized score, in which scores above or below Z = 1.96 are
lated to individual characteristics such as age, education, or less likely to occur by chance (i.e., only in 5 percent of the
sample for a 95 percent CI). A higher percentage than 2.5
general cognitive ability at baseline. Bivariate correlations
were used with bootstrap sampling. The results show a sig- percent (a/2) of improved cases was observed on cognitive
nificant correlation between the improvements in the error flexibility (9 percent), attention/concentration (12 percent to 13
percent) and visual memory (22 percent). These results show
percentage of d2 and the total score of the MoCA ( r = -0.44;
bootstrapped 95 percent CI [-0.23 to -0.74]; SE = 0.13), that there were strong improvements in main domains involved
which suggests that the magnitude of improvements is in the VR/SG program.
The tasks that were used in the cognitive stimulation
highest for individuals with lower levels of cognitive func-
tioning at baseline. program are general tasks that mimic daily life activities but
are not specific, focused tasks for any of these domains.
Discussion However, the specific functions in which significant differ-
ences were observed, that is, attention, memory, and cogni-
Our study was carried out with elderly participants who tive flexibility, are required in daily activities, such as
had not been clinically diagnosed with cognitive deficits. shopping at the supermarket, preparing food, and choosing
the right clothes to wear; in most sessions, these activities
Table 2. Reliable Change Index were used to train participants. Conversely, no significant
differences were observed among the results of the screening
(+) Change (-) Change tests (MoCA and FAB), which assess general functioning;
Z > 1.96 Z < 1.96 this finding suggests that these improvements were restricted
to specific domains of cognitive functioning and are con-
WCST P errors 9 0 sistent with the results of recent reviews showing improve-
RCF memory score 22 0
ments in attention and memory as specific effects of ICT-
d2 errors 12 0
d2 concentration index 13 0 based interventions.16
This finding contrasts with a previous study, in which a
Values are in percentages. similar VR/SG approach was used but in which we used a
6 GAMITO ET AL.

clinical sample diagnosed with cognitive deficits. In that 5. Ballesteros S, Kraft E, Santana S, et al. Maintaining older
study, we found significant improvements in executive func- brain functionality: A targeted review. Neuroscience and
tioning, which was assessed with the FAB.30 However, in that Biobehavioral Reviews 2015; 55:453–477.
study, the sample consisted of patients undergoing community 6. Lampit A, Hallock H, Valenzuela M. Computerized cog-
treatment for alcohol use disorder, which has a different pat- nitive training in cognitively healthy older adults: A sys-
tern of cognitive deficits from the sample in our study. tematic review and meta-analysis of effect modifiers. PLoS
We explored the data set further to determine the rela- Medicine 2014; 11:e1001756.
tionships between the RCIs and individual characteristics 7. Valenzuela M, Sachdev PS. Can cognitive exercise prevent
such as age, education, and general cognitive functioning; the onset of dementia? Systematic review of randomized
the results suggest that the improvements found in attention clinical trials with longitudinal follow-up. The American
Journal of Geriatric Psychiatry 2009; 17:179–187.
(through the decreases in error percentage in d2) were neg-
8. Papp KV, Walsh SJ, Snyder PJ. Immediate and delayed
atively associated with general cognitive functioning at
effects of cognitive interventions in healthy elderly: A re-
baseline. This suggests that if improvements in attention are view of current literature and future directions. Alzheimer’s
the main aim, the most efficient use of this program is to and Dementia 2009; 5:50–60.
target patients showing some signs of cognitive decline. No 9. Gates NJ, Sachdev PS, Fiatarone Singh MF, et al. Cognitive
effects of age or education were found on RCIs within the and memory training in adults at risk of dementia: A sys-
limited range of both in our sample. tematic review. BMC Geriatrics 2011; 11:55.
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Our results should be interpreted with some caution, since 10. Johansson B, Tornmalm M. Working memory training for
our study lacked a control group. We sought to minimize this patients with acquired brain injury: effects in daily life.
problem by transforming the outcomes to RCIs, which is a Scandinavian Journal of Occupational Therapy 2011; 19:
more conservative approach to the analysis of pre-post- 176–183.
treatment effects. This does not allow us to discern the effects 11. Kueider A, Parisi J, Gross A, et al. Computerized cognitive
of practice on repeated test scores. We should note, however, training with older adults: A systematic review. PLoS One
that practice effects are more likely to be seen in measures that 2012; 7:e40588.
involve problem-solving abilities;31 problem-solving was not 12. Gamito P, Oliveira J, Morais D, et al. (2011) Serious games for
required in the evaluations of memory and attention, which serious problems: from Ludicus to Therapeuticus. In Kim JJ,
were assessed using the RCF and the d2, respectively. Also, ed. Virtual reality. London, UK: IntechOpen, pp. 527–548.
the 3-month post-treatment interval may have reduced the 13. Gamito P, Oliveira J, Alghazzawi D, et al. The art gallery
practice effects of repeated exposure to these tests. One way of test: A preliminary comparison between traditional neu-
overcoming this limitation would be to use a standard ropsychological and ecological VR-based tests. Frontiers in
regression-based change score approach from an independent Psychology 2017; 8:1911.
14. Larson EB, Feigon M, Gagliardo P, et al. Virtual reality and
normative group drawn from a different study32 that would
cognitive rehabilitation: A review of current outcome re-
account for practice effects; however, there were no data
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available for most of the tests used in the current study. 15. Pietrzak E, Pullman S, McGuire A. Using virtual reality
The results of our cognitive flexibility, attention, and and videogames for traumatic brain injury rehabilitation: A
memory tests are consistent with recent reviews17,18 and structured literature review. Games for Health Journal
highlight the advantages of using VR/SG for cognitive in- 2014; 3:202–214.
tervention, even with populations that may be unfamiliar 16. Shin HH, Kim KM. Virtual reality for cognitive rehabili-
with the use of such technology, such as the elderly. As tation after brain injury: A systematic review. Journal of
technology keeps progressing, there is great potential for the Physical Therapy Science 2015; 27:2999–3002.
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Author Disclosure Statement cognitive decline: Systematic review of the literature. The
American Journal of Geriatric Psychiatry 2015; 23:335–
No competing financial interests exist.
359.
18. Bogdanova Y, Yee MK, Ho VT, et al. Computerized
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