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339
Clinical Neuropsychiatry (2011) 8, 6,
© 2011 Giovanni Fioriti Editore s.r.l.
339-346
SUBMITTED AUGUST 2011, ACCEPTED DECEMBER 2011
ASSESSING PROCESSING SPEED AND EXECUTIVE FUNCTIONS IN LOW EDUCATED OLDER
ADULTS: THE USE OF THE FIVE DIGIT TEST IN PATIENTS WITH ALZHEIMERS DISEASE,
MILD COGNITIVE IMPAIRMENT AND MAJOR DEPRESSIVE DISORDER
Jonas Jardim de Paula, Rafaela Teixeira de Ávila, Danielle de Souza Costa, Edgar Nunes de Moraes, Maria
Aparecida Bicalho, Rodrigo Nicolato, Humberto Corrêa, Manuel Sedó, Leandro Fernandes Malloy-Diniz
Abstract
Objective: Many studies suggest that executive dysfunction is a common characteristic of Alzheimer´s disease
(AD), mild cognitive impairment (MCI), and in elderly patients with major depressive disorder (MDD). The aim of
this study is to evaluate the applicability of Five Digits Test (5D) in the assessment of executive functions in less
educated older adults with pathological aging.
Method: We studied a total of 114 subjects divided in four groups: 30 patients with AD, 30 patients with MCI, 24
patients with MDD and 30 community-dwelling normal aged controls (NAC). All subjects were submitted to the 5D.
Results: The comparison of NAC and the mixed clinical group (AD + MCI + MDD) shows significant differences
on the 5D both in speed and errors on 3rd (inhibition) and 4th (shifting) sections of the 5D. The ANOVA indicates
significant differences for all measures, except for the total number of errors in the Decoding and Naming components
of the 5D. The Post Hoc analysis indicates that in decoding (time), the NAC group performed better than AD and
MDD but not MCI. MCI patients also performed better than AD. The analysis of components associated with executive
functions of the 5D indicates that NAC outperformed AD and MDD in Inhibition (time) but only AD in Inhibition
(errors) (p<0.016). The Shifting (time) of NAC was faster than MDD, but in the total errors of this component, NAC
the group performed better than AD and MCI.
Conclusions: Our results point to the efficiency of 5D in identifying executive dysfunctions in pathological
aging in comparison with the normal aging process. This task shows great potential for use both in research and in
clinical practices in countries as Brazil, where a great amount of the population is illiterate.
Key words: Alzheimer´s disease, mild cognitive impairment, major depressive disorder, executive dysfunction, five
digits test
Declaration of interest: none
Jonas Jardim de Paula (1), Rafaela Teixeira de Ávila (1), Danielle de Souza Costa (1), Edgar Nunes de Moraes (2), Maria
Aparecida Bicalho (2), Rodrigo Nicolato (3), Humberto Corrêa (3), Manuel Sedó (4), Leandro Fernandes Malloy-Diniz (1,3)
1) Laboratório de Investigações Neuropsicológicas do INCT em Medicina Molecular
2) Departamento de Clínica Médica Faculdade de Medicina/UFMG
3) Departamento de Saúde Mental Faculdade de Medicina/UFMG
4) Omnilingual Tests, Natick Boston
Corresponding author
Jonas Jardim de Paula Mental Health Department - Faculdade de Medicina da Universidade Federal de Minas Gerais
UFMG. Av. Prof. Alfredo Balena, 190
Centro 30130-100 - Belo Horizonte, MG Brasil
jonasjardim@gmail.com
shaped curve (Zelazo et al. 2004). The executive
changes are mediated by a significant decrease in
processing speed and reduced working memory
capacity (Huntley and Howard 2010), a group of
cognitive abilities named cognitive mechanics (Baltes
1997). Education is an important factor in the perfor-
mance of the executive functions among the aging
population. For instance, according to Lin et al. (2007),
although the decline of some components of executive
functions (i.e., attention allocation, planning and
Introduction
Executive functions are capacities that enable a
person to engage successfully in independent,
purposive, self-serving behavior (Lezak et al. 2004).
The development of executive functions occurs during
the maturation of prefrontal networks (Fuster 2009).
This development begins in early childhood and ends
in adolescence and early adulthood, presenting a slow
but consistent decay later in life in an inverted U
340
Jonas Jardim de Paula et al.
Clinical Neuropsychiatry (2011) 8, 6
classified according Clinical Dementia Rating (CDR)
(Morris 1993).
Methods
Participants
We studied a total of 114 subjects divided in four
groups: 30 patients with AD, 30 patients with MCI, 24
patients with MDD and 30 community-dwelling normal
aged controls. The participants were Brazilian older
adults assessed in a secondary public healthcare center
specializing in gerontology. In the city of Belo
Horizonte, where this study was performed, a primary
care physician who assesses older adults in his or her
daily practice could request a specialized assessment
if cognitive decline or dementia was suspected. In the
secondary unit center, the patient was assessed by at
least two gerontologists (ENM and MAB) and one
clinical neuropsychologist (JJP). After the assessments
and complementary exams were performed, clinical
conferral confirms the diagnosis of each patient.
After the diagnosis, the patients were invited to
participate in this study, and there was an interval of no
more than one week between the diagnosis and research
participation. Inclusion criteria were the following: at
least 60 years old, no history of vascular or previous
neurological disorders; no history of depressive disorder
prior 60 years and no confusional status or psychotic
illness. Diagnoses were determined by a consensus
following a multidisciplinary assessment, according to
the DSM-IV (American Psychiatric Association 1994),
NINCDS-ADRDA (McKhann et al. 1984) and NINDS-
AIREN (Román et al. 1993) criteria. For the MCI
diagnosis, the Petersen et al. (2001) criteria were used.
All MDD patients scored above the recommended
cutoff for depression in the Brazilian version of the
Geriatric Depression Scale (Paradela et al. 2005).
All MCI, MDD and AD participants followed their
treatment plans, which included taking cholinesterase
inhibitors, and they were free from typical or atypical
antipsychotic drugs.
All subjects were classified according to the
Clinical Dementia Ratting (0 (NAC), 0.5 (MCI and
MDD) or 1 (mild AD). In the present study, only MDD
patients with self-reported cognitive deficits and
functional impairment were included (CDR=0.5). The
MCI group was composed of 17 amnestic and 13 mul-
tiple domain (amnestic-executive) patients. Patients
with MCI or AD who were also diagnosed with MDD
according to the DSM-IV criteria or another mood
disorder were excluded from the study. All subjects were
assessed in accordance with the Declaration of Helsinki,
and the Research Ethics Committee of the Federal
University of Minas Gerais (334/06) gave written
consent and approval. For AD patients, a relative
(usually spouse) also gave written consent.
Procedures
All subjects performed a protocol composed of a
cognitive and humor screening test and the 5D.
1) Cognitive and mood screening. Cognitive
initiation) is correlated with the aging process,
educational level is more significantly correlated with
the decline of initiation, switching and flexibility, and
online updating.
Many studies suggest that executive dysfunction
is a common characteristic of Alzheimer´s Disease
(AD), even in the early phase (Baudic et al. 2006),
which is associated with episodic memory impairment.
In mild cognitive impairment (MCI), the executive
deficit is a diagnostic criteria for both single domain
executive MCI and multiple domain MCI involving
executive functions. Nonetheless, even in amnestic
MCI, executive deficits may play an important role
because the performance in executive tests may be
affected by the atrophy of medial temporal structures
(Nagata 2010). Executive function deficits are also
observed in elderly patients with major depressive
disorder (MDD), which is associated with gray and
white matter signal abnormalities in the frontal and
medial temporal regions of the brain (Sheline et al.
2006).
Executive function assessment is frequently
performed using classical neuropsychological tools,
such as the Stroop Color Word Test (SCWT) (Stroop
1935), the Trail Making Test (Hervey et al. 2004) or
the Frontal Assessment Battery (Oguro et al. 2006).
These tests are good measures of the executive functions
in subjects with AD, MCI and MDD (Pachana et al.
1996). However, these tasks are influenced by reading
abilities (Johnson et al. 2006) and formal education
(Lucas et al. 2005, Steinberg et al. 2005).
In these situations, an alternative is the Mini-
Verbal Test (MVT), which is designed to be as
independent as possible from the previous experience,
education, and culturally acquired routines of the
subjects. In MVT, the verbal content is limited to a few
familiar concepts, which are presented to the subject
as series of visual images. The main value of this
assessment framework is its use in conditions in which
subjects lack the automatic reading routines that are
absolutely necessary for its validity in the assessment
of illiterate subjects or subjects with very low levels of
education.
The Five Digit Test (5D), proposed by Sedó
(2004), is an MVT adaptation of the SCWT. When
performing this test, the subject must know only the
first five numbers and their corresponding symbols. The
test measures continuous verbal performance at
different levels of the attentional network because it
tests both a more automatic process (i.e., reading
numbers and counting figures) and a more controlled
process, in which the subject must inhibit an
automatized routine of processing in favor of a
secondary, non-intuitive mode of processing (i.e.,
speaking rather than reading the number of digits).
The aim of this study is to evaluate the applicability
of 5D in the assessment of executive functions in less
educated older adults with AD, MCI and MDD by
evaluating the following hypothesis: (1) the 5D test will
be a useful task in the assessment of executive functions
in elderly population. Therefore, we expect that subjects
affected by AD, MCI or MDD will perform poorly on
the 5D compared to normal aged controls; (2) the per-
formance in the 5D will be associated with a greater
degree of general cognitive and functional impairment
341
Use of the Five Digit Test in Alzheimers disease, Mild Cognitive Impairment and Major Depressive Disorder
Clinical Neuropsychiatry (2011) 8, 6
We considered as statistically significant results where
p ≤0.05. The statistical analysis was conducted using
the SPSS 17.0 software.
Results
We studied a total of 114 subjects divided in four
groups: 30 patients with AD (12 males, age: 74.36 years
± 6.79, education: 3.85 years ± 3.0), 30 patients with
MCI (13 males, age: 74.07 years ± 6.33, education: 4.57
years ± 3.00), 24 patients with MDD (5 males, age:
70.12 years ± 8.54, education 4.13 years ± 3.0) and 30
community-dwelling normal aged controls (10 males,
age: 74.10 years ± 6.80, education: 4.27 years ± 2.25).
No significant differences were found between age
(p=0.093), education (p=0.793), and sex (p=0.335)
between the groups. The demographics and
neuropsychological tests results are shown in table 1.
Table 1 shows the mean and standard deviations for
the demographics, GDS, MMSE, the four components
of 5D, and the significance of ANOVA and effect size
for each group comparison.
The comparison of NAC and the mixed clinical
group shows no differences in age (p=0.481), education
(p=0.889) and gender (p=0.815). Significant differences
(p<0.001) were found in MMSE and GDS-15 with large
effect sizes (1.45, and 0.79, respectively). On the 5D,
the Decoding (p<0.001; d=0.73) and Describing
(p<0.001; d=0.72) times were different, but the number
of errors was not different (p=0.169 and p=0.109).
Considering both time and errors on 3rd (inhibition) and
4th (shifting) sections of the 5D, we also found
statistically significant differences between groups with
large effect sizes [Inhibition time (p<0.001 d=0.62) and
errors (p=0.001 d=056); Shifting time (p<0.003 d=0.52)
and errors (p<0.001 d=0.66)].
In the AD group, 1 patient was unable to execute
the Inhibition component of the 5D, and 10 patients
were unable to execute the Flexibility component
(χ²=22.5 p<0.001), a pattern different from each of the
other three groups, in which all the patients performed
all of the 5D components. The ANOVA indicates
significant differences for all of the neuropsychological
measures, except for the total number of errors in the
Decoding and Naming components of the 5D. The effect
sizes of the comparisons were moderate to large,
ranging from 0.081 (Inhibition Errors) to 0.190
(Describing Time). These results are shown in table 1
and figure 2.
The Post Hoc analysis of the 5D indicates that in
Decoding (time), the NAC group performed better than
AD (p<0.001) and MDD (p<0.018) but not MCI
(p=0.687). MCI patients also performed better than AD
(p=0.036). In the Decoding (errors) analysis, no group
differences were found. In Describing (time) the NAC
group showed a similar pattern, with faster times than
AD (p=0.005) and MDD (p=0.027) but not MCI
(p=0.920). No differences were found between
Describing (errors). The analysis of components
associated with executive functions of the 5D indicates
that NAC outperformed AD (p=0.020) and MDD
(p=0.014) in Inhibition (time) but only AD in Inhibition
(errors) (p<0.016). The Shifting (time) of NAC was
faster than MDD (p=0.005), but in the total errors of
screening was performed by the use of Mini-Mental
State Exam (MMSE), a widely used screening test
developed by Folstein, Folstein and McHugh (1975).
Using 11 simple tasks, the MMSE evaluates temporal
orientation, spatial memory, attention, language and
praxia. The current study employed a Brazilian version
with different cutoffs based on education (Brucki et al.
2003). The Geriatric Depressive Scale (GDS) was used
for screening depressive symptoms in our sample. In
this study, we used the Brazilian version of the GDS-
15 (Paradela et al. 2005).
2) The five Digit Test: 5D is divided into four suc-
cessive parts: 1) decoding, 2) describing, 3) inhibiting
and 4) shifting. Each part involves the production of
four identical verbal lists, using the activities of reading,
describing, choosing, and switching. All parts of the
test were preceded by a training session containing 10
items. After the instructions, the subject had four trials
to correctly respond to the items. If the subject was
unable to perform at the training session, these data are
registered, and the test components that followed the
interruption were excluded from the statistical analysis.
The items of each parts were presented in pages
of 50 items (10 rows of five items), and each item was
surrounded by a rectangular frame. On the first section,
in the decoding section of the test, the subject is
presented with a series of 50 boxes that require the
automatic reading of the items inside each box, which
are in groups of one to five congruous digits (one 1,
two 2s, three 3s, etc.) that must be read. In the second
section (the retrieving section), the subject is presented
with a series of 50 boxes, in which one to five stars
must be counted. In the third section (the inhibition
section), digits are presented in incongruous forms (one
4, two 3s, five 1s, etc.), and the subject is asked to report
the number of digits, and so must inhibit his or her
immediate reaction (reading) and resolve to count the
number of digits presented and continue counting them
throughout the page. Finally, in the fourth section (the
shifting section), of the test, the subject is presented
with an additional difficulty: he or she must switch from
counting to reading in 20% of the items of the page
(the items marked by a much darker frame), demanding
the more executive process of shifting. In each of the
four sections of the 5D, we measured the subjects speed
of information processing (reading time in seconds) and
the efficiency of their responses (number of errors).
Figure 1 shows the four test components.
Analyses
For the test of Hypothesis 1, the comparisons of
the NAC group and the mixed clinical group (MCG)
were carried out by independent-samples paired t tests,
and a modified Cohens d appropriated for unequal
sample sizes (Hartung et al. 2008) was used as a
measure of effect size. The statistical analyses of
Hypothesis 2 consisted of a One-Way Analysis of
Variance (ANOVA) for the group comparisons, using
Sidaks Post Hoc to evaluate specific group differences
because it offers a more conservative approach,
minimizing the chance of type 1 errors in multiple
comparisons (Ruxton and Beauchamp 2008). The
squared eta was calculated as an estimate of effect size.
342
Jonas Jardim de Paula et al.
Clinical Neuropsychiatry (2011) 8, 6
Figure 1. Examples of 5d components
Figure 2. Comparison among NAC, MCI, AD and MDD in 5D (time to complete Decoding, Retrieving, Inhibiting
and Shifting parts)
343
Use of the Five Digit Test in Alzheimers disease, Mild Cognitive Impairment and Major Depressive Disorder
Clinical Neuropsychiatry (2011) 8, 6
Table 1. Demographics and neuropsychological tests results and comparisons among MCG, NAC, AD, MCI AND
MDD
this component, NAC the group performed better than
AD (p=0.022) and MCI (p=0.046). No other group
differences were found.
To further analyze the differences in executive
functions among the groups, an interference score was
computed subtracting the Decoding time from the
Inhibition and Shifting time. The aim of this procedure
was to minimize the influence of processing speed on
executive performance, creating a more one-
dimensional measure. No differences between the
Interference-Inhibition (p=0.573) and Interference-
Shifting (p=0.326) were found in the test of H1 or in
Interference-Inhibition (p=0.096) and Interference-
Shifting (p=0.201) in H2.
Discussion
This study evaluated the efficiency of 5D in the
assessment of executive functions in less educated older
adults with AD, MCI and MDD. Our findings show
that the 5D may be a useful neuropsychological
assessment tool for elderly patients with cognitive
impairments. When a mixed clinical group is compared
with the 5D, differences among the task components
appear to be more related to processing speed (Decoding
and Describing time), with large effect sizes,
corroborating the discrepancy between the speed of
performance of patients and controls. Processing speed
declines with age (Salthouse 2000, Salthouse 2003,
Brown et al. 2011), and older individuals tend to present
a greater variability in performance (Salthouse 1998).
Differences among clinical groups and healthy subjects
are usually related (Wadley et al. 2011). As suggested
by Boone et al. (1998), the performance results of mul-
tiple executive functions tend to show a moderate
association, indicating a common structure and the
presence of more specific components. In Boones
analysis, the SCWT had shared factorial loadings with
the Digit Symbol task of the Wechsler Intelligence
Scales, indicating that processing speed is related to
the Inhibition process of the Stroop task.
The effect sizes of executive components were
moderate to high, and differences in efficiency were
found, suggesting that the executive process may also
be compromised. Similar results were found using the
SCWT in head-injury patients (Rios et al. 2004,
Felmingham et al. 2004) and patients with Alzheimers
Disease (Spieler et al. 1996, Bondi et al. 2002);
however, in MCI and MDD, recent studies have found
no difference in the Inhibition time in Stroop Tasks
(Zhang et al. 2007, Kertzman et al. 2010). It is important
D' E D/ D
D ^ D ^ D ^ D ^ D ^ EKs
^
'^
DD^
d
d
/ d
/
^ d
^
D' D ' E E D/ D / DD
344
Jonas Jardim de Paula et al.
Clinical Neuropsychiatry (2011) 8, 6
to emphasize that interference scores from Stroop tasks
may not be simple measures of inhibition. Salthouse
and Meinz (1995) found that different measures of
inhibition share most of their age-related variance with
other measures of processing speed. Despite the
proportion of shared age-related variance, they
suggested that specific effects could be accurately
estimated when the effects associated with the common
influence are first controlled. As previously mentioned,
the impairment of executive functions is not the core
neuropsychological impairment found in MCI, AD and
MDD, so a severe impairment was not expected in our
sample, which may explain the more significant
processing speed impairments.
Our data suggest that the processing speed
impairments may be a more consistent finding in dif-
fuse neurological damage, dementia or chronic mood
disorders (Selnes and Vinters 2006, Duering et al. 2011,
Brown et al. 2011, Burdick et al. 2010). As previously
argued, the three clinical conditions examined in our
study show white matter abnormalities (Alexopoulos
et al. 2008, Douaud et al. 2011), which may mediate
this cognitive deficit. According to this hypothesis,
some evidence is provided by studies that show that
processing speed may be secondary to a loss of integrity
in white matter connection fibers (Fry and Hale 2000,
Hansell et al. 2005, Rypma et al. 2005, Jung and Haier
2007, Turken et al. 2011). Penke et al. (2010) has shown
that the general integrity factor of white matter is
associated with a series of cognitive abilities, including
processing speed, intelligence, and memory. Turken et
al. (2011) also found a positive correlation between the
structure of white matter pathways and processing speed
in a healthy population and left hemisphere lesion
patients. Although processing speed is not correlated
with a specific brain region, the role of white matter in
integrating information across spatially distinct brain
regions suggests that cognitive slowing is related to
neuronal efficiency. This hypothesis shows significant
ecological validity because the impairments in
processing speed are associated with greater functional
deficits and may be used as estimates of MCI
conversion to dementia (Tabert et al. 2002, Devanand
et al. 2008).
When comparing the degrees of general cognitive
and functional impairment, the performance in the 5D
was not associated with a higher CDR score. Different
clinical conditions can imply a marked slowness of
performance in all test situations, especially controlled
situations that require further use of voluntary self-
direction, persistence and mental effort, and a greater
resilience to the presence of stress and fatigability
(Nathan et al. 2001). Normally, healthy older adults
show declined performances in processing speed,
inhibition and flexibility (Zelazo et al. 2004), three
components of the 5D. This pattern may be influenced
by general slowing difficulties associated with aging
but tends to be more accentuated in clinical conditions,
such as dementia. In AD patients, as suggested by Bondi
et al. (2002), the slowness and magnitude of interference
increases with the severity of dementia. The analysis
of our second hypothesis revealed a discrepancy in
performance of the four groups studied in all of the 5D
components, excluding the total errors in Decoding and
Describing, with moderate to high effect sizes. The Post
Hoc analysis indicating that the CDR associated
declines, however, was not supported by our data. In
the Decoding and Describing Times, no differences
were found between the NAC and MCI groups, but
differences were present in NAC and MDD. MCI
patients also performed better than AD. NAC patients
were no faster than MCI in Inhibition and Shifting times
but again had better performance than AD and MDD in
Inhibition Time and better performance than MDD in
Shifting Time. The efficiency of Inhibition of AD
patients was inferior compared to the NAC group but
not MCI and MDD, although in Flexibility, NAC
outperformed MCI and AD patients. These results do
not support our second hypothesis, but the Shifting
differences encountered in terms of efficiency should
be better evaluated in future studies. It must be
considered that in the present study, the MCI sample is
predominantly of the amnestic type, minimizing the
degree of impairment expected in executive functions
and processing speed. The small sample size may also
be an important bias for these observations.
The poor performance of AD patients in Stroop
Tasks is well documented in the neuropsychological
literature (Bondi et al. 2002, Spieler et al. 1996, Perry
and Hodges 1999, Perry et al. 2000). Our result, using
an MVT task variation, corroborates this pattern,
indicating convergence validity of the two tasks in a
clinical sample. These results are consistent with those
presented by Sedó and DeCristoforo (2001), where
moderate to high correlations were found between the
SCWT and the 5D in a healthy North American older
adult sample, and those obtained by Hsieh et al. (1996)
and Hsieh and Tori (2007) in a Chinese elderly
population. In our sample, an important fact that may
be used as a clinical guideline for older adults
assessment is that NAC, MCI and MDD patients
matched by age, education and gender to AD patients
were able to complete all of the 5D components,
although 10 of 30 AD patients were unable to perform
the Shifting component and only one the Inhibition
component. This cognitive shifting deficit may be a
more specific feature of the AD neuropsychological
deficits, which is also corroborated by the greater
efficiency impairment with relative preservation of
speed, in a fast but inaccurate performance, typical of
executive impairments (Kogan 1971). Balota et al.
(2010) showed, for example, that the errors on
incongruent trials were the best discriminator of those
who converted and those who did not convert to AD
over a 14-year period.
Our results point to the efficiency of 5D in
identifying executive dysfunctions in pathological aging
in comparison with the normal aging process.
Furthermore, the assessment of cognition in less
educated elderly subjects needs to consist of appropriate
stimuli (i.e., stimuli that do not require reading or
writing abilities). This task shows great potential for
use both in research and in clinical practices. Drawbacks
in instruments, such as the chromatic (Lezak et al.
2004), visual (Dyer 1973, Spreen and Strauss 1998),
and linguistic (Cox et al. 1997) properties of the SCWT,
have limited their application in clinical special-needs
contexts, where difficulties in color perception, visual
impairments, specific reading problems, and language
disorders are presented. This is the recurrent profile of
345
Use of the Five Digit Test in Alzheimers disease, Mild Cognitive Impairment and Major Depressive Disorder
Clinical Neuropsychiatry (2011) 8, 6
the elderly in Brazil, where 26% of the population is
illiterate (IBGE 2009). In these contexts, the MVT tests
appear to be an appropriate choice for the assessment
of processing speed and executive functions.
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