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Geriatr Gerontol Int 2014
ORIGINAL ARTICLE: SOCIAL RESEARCH,
PLANNING AND PRACTICE
Influence of depression, anxiety and stress on cognitive
performance in community-dwelling older adults living in
rural Ecuador: Results of the Atahualpa Project
Oscar H Del Brutto,1,2 Robertino M Mera,3 Victor J Del Brutto,4 Gladys E Maestre,5
Hannah Gardener,6 Mauricio Zambrano4 and Clinton B Wright6
School of Medicine, Universidad Espíritu Santo – Ecuador, 2Department of Neurological Sciences, Hospital-Clínica Kennedy, Guayaquil,
Community Center, Atahualpa, Ecuador; 3Gastroenterology Department, Vanderbilt University, Nashville, Tennessee, 5Departments of
Psychiatry and Neurology, and Gertrude H. Sergievsky Center, Columbia University, New York, New York, and 6McKnight Brain Institute
and Department of Neurology, Miller School of Medicine, University of Miami, Miami, Florida, USA
1
4
Aim: To assess the relationship between cognitive status and self-reported symptoms of depression, anxiety and
stress of older adults living in an underserved rural South American population.
Methods: Community-dwelling Atahualpa residents aged ≥60 years were identified during a door-to-door census,
and evaluated with the Depression Anxiety Stress Scale-21 (DASS-21) and the Montreal Cognitive Assessment
(MoCA). We explored whether positivity in each of the DASS-21 axes was related to total and domain-specific MoCA
performance after adjustment for age, sex and education.
Results: A total of 280 persons (59% women; mean age, mean age 70 ± 8 years) were included. Based on established
cut-offs for the DASS-21, 12% persons had depression, 15% had anxiety and 5% had stress. Mean total MoCA
scores were significantly lower for depressed than for not depressed individuals (15.9 ± 5.5 vs 18.9 ± 4.4, P < 0.0001).
Depressed participants had significantly lower total and domain-specific MoCA scores for abstraction, short-term
memory and orientation. Anxiety was related to significantly lower total MoCA scores (17 ± 4.7 vs 18.8 ± 4.5,
P = 0.02), but not to differences in domain-specific MoCA scores. Stress was not associated with significant differences in MoCA scores.
Conclusion: The present study suggests that depression and anxiety are associated with poorer cognitive performance in elderly residents living in rural areas of developing countries. Geriatr Gerontol Int 2014; ••: ••–••.
Keywords: anxiety, Atahualpa, cognitive decline, depression, developing countries, Ecuador, Montreal Cognitive
Assessment, population-based study.
Introduction
The prevalence of mild cognitive impairment (MCI) and
dementia is growing at an alarming rate among older
adults living in many low- and middle-income countries.1 In addition, the contribution of psychiatric and
neurological disorders to the total burden of illness has
increased almost threefold in Latin America during the
past few years.2 Accurate estimates of the numbers of
Accepted for publication 30 March 2014.
Correspondence: Dr Oscar H Del Brutto MD, Air Center 3542,
PO Box 522970, Miami, Fl 33152-2970. Email:
[email protected]
© 2014 Japan Geriatrics Society
persons with MCI and dementia are necessary for public
health planning in these underserved populations.
However, such assessment might be complicated by
cross-cultural factors and illiteracy, which could make
some of the most widely-used screening instruments
non-reliable.3
Depression, anxiety and stress are extremely common
functional disorders that interfere with quality of life,
and might trigger or worsen a number of medical conditions that are detrimental to health. The relationship
between psychological distress, especially depression,
and cognitive decline has been extensively evaluated in
developed countries,4 but the effects of this association
have been less well studied in most middle- and lowincome countries. People living in these regions do not
doi: 10.1111/ggi.12305
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OH Del Brutto et al.
seek medical attention for depression or anxiety, which
they considered as a normal part of their lives, or even a
proxy for a better socioeconomic status.5
Regional epidemiological surveys could provide
useful insights into the impact of psychological distress
on cognition in rural populations of developing countries. In the present study, we take advantage of the
uniqueness of the Atahualpa Project to assess the influence of symptoms related to depression, anxiety and
stress on the cognitive performance of older adults
living in a village that is representative of rural Ecuador.6
Better understanding of the problem would allow public
health administrators to develop cost-effective strategies
for reducing the burden of MCI and dementia.
Methods
Study population
Atahualpa is located in coastal Ecuador, and more than
95% of the population belongs to the Native/Mestizo
ethnic group (Amerindians). Its residents have better
cardiovascular health than people in urban centers as a
result of their rural lifestyle.7 Crime rates are low, inhabitants do not migrate and a sizable proportion of them
have never even visited large urban centers, which are
more than 100 km apart.
Study design
Ethics considerations of the study and informed
consent forms were approved by the institutional
review board of Hospital-Clínica Kennedy, Guayaquil,
Ecuador. Trained field personnel – including general
physicians – carried out a door-to-door survey to identify all Atahualpa residents aged ≥60 years, defined as
those persons who had lived in the community for the
3 months preceding the start of the survey (15 June
2013). A standard field instrument was used to assess
sociodemographic characteristics, including age, sex,
race/ethnicity, education and occupation. Consenting
individuals were then evaluated by questionnaires that
assessed symptoms consistent with depression, anxiety
and stress, as well as cognitive status.
Cognitive performance was assessed using the
Spanish version of the Montreal Cognitive Assessment
(MoCA) test (http://www.mocatest.org; © Z Nasreddine
MD, version 7 November 2004). The MoCA evaluates
major cognitive domains: visuospatial-executive (trail
making B task, 3-D cube copy and clock drawing) for a
maximum of 5 points; naming (unfamiliar animals) for a
maximum of 3 points; language (sentence repetition and
a phonemic fluency task) for a maximum of 3 points;
short-term memory (delayed recall or words) for a
maximum of 5 points; abstraction (verbal abstraction)
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for a maximum of 2 points; attention and calculation
(digits forward and backward, target detection using
tapping, serial 7s subtraction) for a maximum of 6
points; and orientation (time and space) for a maximum
of 6 points.8
The Depression Anxiety Stress Scale (DASS-21) provided quantitative measures of depression (dysphoria,
hopelessness, devaluation of life, self-deprecation, lack
of interest/involvement, anhedonia and inertia), anxiety
(autonomic arousal, skeletal muscle effects, situational
anxiety and subjective experience of anxious affect) and
stress (chronic non-specific arousal, difficulty relaxing,
nervous tension, and being easily upset, irritable and
intolerant). The DASS-21 is a reliable field instrument
comprising three sets of questions (seven in each set).
The responses are rated on a four-point Likert scale
ranging from 0 (not at all) to 3 (almost always) with a
maximum total score of 21 for each axis.9
As people living in Atahualpa speak Spanish, we used
the validated Spanish version of the MoCA that is
posted on the original web site as developed by Z
Nasreddine (http://www.mocatest.org/), and previously
tested in other Spanish-speaking communities of South
America, including Atahualpa.10,11 We did not use a
cut-off score for defining cognitive impairment, but the
continuous MoCA score (total and domain-specific) to
compare performance in the test across persons with
and without psychological distress, to avoid problems
related to poor reliability of specific cut-offs in less welleducated populations.10,11 The DASS-21 questionnaire
was independently translated and back-translated from
its original English version to Spanish by bilingual physicians from our group (OHD and GEM). Disagreements in translation were resolved through discussion
and consensus. Then, the Spanish version of the
DASS-21 was culturally adapted – including vernacular
Spanish words used by local people – with the aid of
Atahualpa’s community leaders and rural doctors that
had been working in the village, and tested in a random
sample of the population before the study
Statistical analyses
Descriptive statistics are presented as means with standard deviations for continuous variables and as percentages for categorical variables. We examined the
associations between demographic variables (age, sex,
education) and each of the axes of the DASS-21 with
the total MoCA score using linear regression, and with
the domain-specific scores using ordinal logistic
regression. Univariate analyses were examined, and we
evaluated the relationship between each of the axes of
the DASS-21 with total and domain-specific MoCA
scores after adjustment for age, sex, and education. All
analyses were carried out using STATA software version
13 (STATA Corp, College Station, TX, USA).
© 2014 Japan Geriatrics Society
© 2014 Japan Geriatrics Society
102 (36.4)
52 (18.6)
57 (20.4)
41 (14.6)
16 (5.7)
12 (4.3)
–
14 (5.0)
36 (12.9)
230 (82.1)
–
–
–
–
75 (26.8)
120 (42.9)
54 (19.3)
31 (11.1)
–
–
–
21 (7.5)
30 (10.7)
43 (15.4)
44 (15.7)
56 (20.0)
55 (19.6)
31 (11.1)
3 (1.1)
26 (9.3)
76 (27.1)
108 (38.6)
46 (16.4)
21 (7.5)
–
0
1
2
3
4
5
6
37 (13.2)
67 (23.9)
106 (37.9)
70 (25.0)
–
–
–
Short-term memory
n (%)
Abstraction
n (%)
Language
n (%)
Attention/calculation
n (%)
Naming
n (%)
Visuospatial-executive
n (%)
Score
Table 1 Distribution of scores across cognitive domains in 280 Atahualpa residents aged ≥60 years
The door-to-door census identified 323 Atahualpa residents aged ≥60 years, of whom 17 declined to participate. A total of 26 persons were additionally excluded
because of severe visual impairment (14 cases), deafness
(6 cases) or aphasia (6 cases), which prevented them for
completing the MoCA or the DASS-21. The 280 participants included 116 men and 164 women with a
mean age of 70 ± 8 years. Of the 116 men, 90 were
actively working (58 as carpenters) and 26 were retired.
Of the 164 women, 135 were homemakers, 26 remained
at home, but were not involved in caregiving activities,
and just five worked outside the home. Mean school
years of the entire group was 6 ± 3 years. A total of 227
(81%) of participants only completed primary school or
less, and 53 had secondary school education or higher.
The mean MoCA score was 18.5 ± 4.6 for the whole
study group (including an extra point given for education
of ≤12 years in 271 out of 280 persons). Table 1 shows
the distribution of scores across the specific domains of
cognition. Total MoCA performance was better for
persons aged 60–74 years, for men of all ages and for
those with secondary school education or higher.
Younger participants had higher scores in all specific
cognitive domains except abstraction. Men had higher
scores than women in naming, attention/calculation and
language domains, whereas women had better shortterm memory scores. More educated persons scored
higher in the domains of language, short-term memory,
naming and attention/calculation (Table 2).
Results in the DASS-21 indicated that 33 individuals
had depression, 41 had anxiety and 14 had stress.
Depression was more common in women than in men,
but was not influenced by age or education. Patients
with anxiety were older than those without anxiety and
were more frequently women, but anxiety was not influenced by education. Stress was not influenced by age,
sex or education.
Participants with depression had significantly lower
total MoCA scores and significantly lower scores for
short-term memory, attention/calculation and orientation than non-depressed participants (Table 3). Participants with anxiety also had lower total MoCA scores
and significantly lower scores for orientation than nonanxious participants. Stress did not influence total
MoCA scores, but stressed participants had significantly
lower scores for orientation.
Table 4 shows the results of the multivariable model,
with the total MoCA score as a dependent variable and
adjusted for age, sex and education, confirmed that participants with depression had significantly lower total
MoCA scores (P = 0.006) and domain-specific scores
for abstraction, short-term memory, and orientation
than non-depressed participants. A multivariable model
with anxiety score as a continuous variable, and after
Orientation
n (%)
Results
–
1 (0.4)
3 (1.1)
11 (3.9)
39 (13.9)
81 (48.2)
145 (51.8)
Cognitive performance and psychological distress
|
3
4
|
15.7 ± 4.6
0.43 (0.26–0.71)
0.47 (0.29–0.78)
0.28 (0.17–0.46)
0.54 (0.32–0.89)
1.22 (0.59–2.54)
0.42 (0.25–0.69)
0.34 (0.20–0.57)
19.4 ± 4.2
Ref
Ref
Ref
Ref
Ref
Ref
Ref
MoCA total, max 30
(mean ± SD)
Visuospatial-executive
(max 5)
Naming (max 3)
Attention/calculation
(max 6)
Language (max 3)
Abstraction (max 2)
Short-term memory
(max 5)
Orientation (max 6)
Ref
Ref
Ref
Ref
<0.0001
Ref
Ref
Ref
19.6 ± 4.1
Sex
Men
(n = 116)
0.02
0.59
0.001
0.003
<0.0001
0.001
0.0001
P-value
(age)
0.76 (0.49–1.20)
0.65 (0.42–1.00)
1.03 (0.56–1.91)
1.55 (1.01–2.39)
0.27 (0.17–0.43)
0.30 (0.19–0.46)
0.88 (0.57–1.35)
17.7 ± 4.8
Women
(n = 164)
0.25
Ref
Ref
Ref
Ref
Ref
Ref
<0.0001
<0.0001
0.05
0.92
0.04
Ref
17.9 ± 4.6
Education
Primary
(n = 227)
0.55
0.001
P-value
(sex)
1.36 (0.76–2.42)
3.59 (2.05–6.30)
1.61 (0.68–3.86)
2.58 (1.50–4.42)
3.20 (1.81–5.66)
2.85 (1.66–4.90)
1.68 (0.97–2.89)
21.3 ± 3.7
Secondary
(n = 53)
0.30
<0.0001
0.28
0.001
<0.0001
0.0001
0.06
0.0001
P-value
(education)
Ref
Ref
Ref
Ref
1.15 (0.59–2.24)
2.24 (1.00–5.02)
2.81 (1.39–5.66)
2.81 (1.44–5.48)
0.003
0.68
0.05
0.004
0.14
0.03
0.08
<0.0001
P-value
(depression)
1.95 (1.06–3.60)
1.57 (0.85–2.91)
1.67 (0.77–3.64)
1.60 (0.87–2.94)
1.28 (0.70–2.33)
1.72 (0.96–3.09)
1.05 (0.58–1.91)
17 ± 4.7
Anxiety
Anxious
(n = 41)
Ref
Ref
Ref
Ref
Ref
Ref
Ref
18.8 ± 4.5
Nonanxious
(n = 239)
0.03
0.15
0.20
0.13
0.42
0.07
0.88
0.019
P-value
(anxiety)
2.74 (1.03–7.27)
1.83 (0.67–4.97)
1.42 (0.40–5.07)
1.96 (0.72–5.39)
0.89 (0.34–2.36)
1.55 (0.60–3.99)
1.00 (0.38–2.65)
16.7 ± 5.1
Stress
Stressed
(n = 14)
Ref
Ref
Ref
Ref
Ref
Ref
Ref
18.6 ± 4.6
Nonstressed
(n = 266)
0.04
0.24
0.59
0.19
0.81
0.36
1.00
0.135
P-value
(stress)
Data presented as odds ratio (95% confidence interval) per 1 point score increase, unless otherwise stated. Max, maximum score; MoCA, Montreal Cognitive Assessment;
Ref, reference group.
Ref
Ref
Ref
1.80 (0.93–3.48)
1.64 (0.85–3.16)
2.04 (1.08–3.88)
18.9 ± 4.4
15.9 ± 5.5
MoCA total, max 30
(mean ± SD)
Visuospatial-executive
(max 5)
Naming (max 3)
Attention/calculation
(max 6)
Language (max 3)
Abstraction (max 2)
Short-term memory
(max 5)
Orientation (max 6)
Nondepressed
(n = 247)
Depression
Depressed
(n = 33)
Scores
Table 3 Comparison of total and domain-specific Montreal Cognitive Assessment for participants with and without depression, anxiety and stress
Data presented as odds ratio (95% confidence interval) per 1 point score increase, unless otherwise stated. Max, maximum score; MoCA, Montreal Cognitive Assessment;
Ref, reference group.
≥75 years
(n = 70)
Age
60–74 years
(n = 210)
Scores
Table 2 Total and domain-specific Montreal Cognitive Assessment scores in relation to age, sex and education
OH Del Brutto et al.
© 2014 Japan Geriatrics Society
© 2014 Japan Geriatrics Society
Data presented as odds ratio (95% confidence interval) per 1 point score increase, unless otherwise stated. Max, maximum score; MoCA, Montreal Cognitive Assessment;
Ref, reference group.
0.11
0.90
0.79
0.36
0.22
0.61
0.24
0.03
Ref
Ref
Ref
Ref
Ref
Ref
Ref
Ref
(1.13)
(0.40–2.82)
(0.32–2.37)
(0.61–4.05)
(0.68–5.16)
(0.39–5.00)
(0.67–5.20)
(1.15–8.23)
1.80
1.06
0.87
1.57
1.88
1.40
1.86
3.08
0.23
0.74
0.59
0.82
0.48
0.17
0.14
0.14
Ref
Ref
Ref
Ref
Ref
Ref
Ref
Ref
(0.71)
(0.49–1.66)
(0.45–1.57)
(0.59–1.95)
(0.67–2.35)
(0.79–3.95)
(0.86–3.02)
(0.86–3.01)
0.85
0.90
0.84
1.07
1.25
1.77
1.61
1.61
0.01
0.18
0.70
0.20
0.79
0.05
0.002
0.01
Ref
Ref
Ref
Ref
Ref
Ref
Ref
Ref
2.10
1.58
1.14
1.53
0.91
2.29
3.08
2.58
MoCA total max 30, (beta [SE])
Visuospatial-executive (max 5)
Naming (max 3)
Attention/calculation (max 6)
Language (max 3)
Abstraction (max 2)
Short-term memory (max 5)
Orientation (max 6)
(0.77)
(0.81–3.10)
(0.58–2.24)
(0.80–2.94)
(0.46–1.80)
(1.00–5.23)
(1.49–6.39)
(1.31–5.09)
NonP-value
stressed (stress)
(n = 266)
Stress
NonP-value Stressed
anxious (anxiety) (n = 14)
(n = 239)
Anxiety
NonP-value
Anxious
depressed (depression) (n = 41)
(n = 247)
Depression
Depressed
(n = 33)
Scores
Table 4 Associations of depression, anxiety, and stress with total and domain-specific Montreal Cognitive Assessment scores, adjusting for age, sex and
education
Cognitive performance and psychological distress
adjusting for age, sex and education, showed that
anxious participants had significantly lower total MoCA
scores than non-anxious participants (difference = 2
SD; P = 0.026). Results of the multivariable model with
the stress score as a continuous variable, and after
adjustments for age, sex and education, showed that
stressed participants only had significantly lower scores
for orientation (P = 0.03).
Discussion
The results of the present study showed that selfreported symptoms of depression and anxiety have an
adverse influence on performance in cognitive testing,
and are related to significant reductions in mean values
of total MoCA score. Scores in some specific domains of
cognitive functions, including short-term memory,
attention/calculation and orientation, are also negatively
influenced by depression.
The relationship between psychological distress and
cognitive decline is bidirectional and complex.12 The
causal relationship between these conditions remains
uncertain, because the prevalence of both increases with
advancing age, and there is a paucity of prospective
studies.13 Some studies have found that depression does
not precede cognitive decline,14,15 whereas others concluded that depression is a risk factor for incident
dementia.16,17 Irrespective of whether depression
co-occurs with or leads to cognitive impairment, it is
important to recognize the detrimental effect on the
performance in cognitive screening tests that occur in
persons with psychological distress.
Most field instruments used to detect cognitive
impairment were created and used in developed countries, where people have higher levels of education than
in the developing world. These tests might overestimate
the prevalence of cognitive impairment in subjects from
rural areas of developing countries, who have low literacy but are functioning normally within their native
environment.10 Lower cut-off scores for cognitive
impairment or the use of tests that are less influenced by
literacy have been proposed for these populations.18,19
However, there has been no attempt to correct for the
impact of psychological distress on cognition. The
present results suggest that adjustments of already
established cut-off scores for individuals with depression or anxiety are indeed necessary to avoid overestimation of cognitive impairment in rural populations of
developing countries.
In general, responsibilities placed on persons living in
rural areas are not as high as in those living in the urban
setting, where pressure to achieve a higher socioeconomic status often comes at the price of increased levels
of depression and anxiety. Nevertheless, depression
and anxiety could also exist at the rural level, and its
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OH Del Brutto et al.
occurrence might adversely influence performance in
cognitive testing among community-dwelling older
adults. Community-based surveys carried out in underserved populations have shown prevalence rates of geriatric depression ranging from 11% to 13%,20–22 which
are similar to that found in the present survey. Most of
these studies, however, have not assessed the prevalence
of anxiety and stress, and have not correlated the occurrence of psychological distress with cognitive status. In
this regard, the present study is unique as it assessed the
prevalence of the different axes of psychological distress
and their correlation with cognitive performance in an
unbiased population of community-dwelling older
adults living in a rural village.
Psychological distress and cognitive impairment in
the elderly could be related to cerebrovascular disease.23
We did not evaluate that possibility in our study as a
result of the small number of persons with a clinically
overt stroke, and because some of our stroke patients
were not enrolled because aphasia prevented them for
completing the MoCA or the DASS-21. An ongoing
study in which all community-dwelling older adults
living in Atahualpa will be studied with magnetic resonance imaging will allow determining whether silent
strokes, asymptomatic white matter lesions or cardiovascular risk factors could account for some cases of
psychological distress or poor performance in cognitive
tests. In addition, as we assessed psychological distress
and cognition in a cross-sectional survey, the present
results cannot confirm whether the former was the
cause or the result of poor cognitive performance, and
this could be a potential limitation of our study. Nevertheless, the present results strongly support adjustment of cut-off scores used to evaluate cognitive decline
in the presence of depression or anxiety. Longitudinal
studies in these underserved populations are required to
show the cause-and-effect relationship of the association between psychological distress, cognition and cerebrovascular disease.
Acknowledgement
This study was partially supported by an unrestricted
grant from Universidad Espíritu Santo – Ecuador,
Guayaquil – Ecuador.
Disclosure statement
The authors declare no conflict of interest.
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