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The Effect of Education on Age-Related Changes

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The Effect of Education on Age-Related Changes in

Three Cognitive Domains: A Cross-Sectional Study in
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a a a a
Isabel Pavão Martins , Carolina Maruta , Cláudia Silva , Pedro Rodrigues , Catarina
a a a a b
Chester , Sandra Ginó , Vanda Freitas , Sara Freitas & António Gouveia Oliveira
a
Language Research Laboratory, Institute of Molecular Medicine and Faculty of Medicine,
University of Lisbon, Lisbon, Portugal
b
Department of Biostatistics, Faculty of Medical Sciences, Universidade Nova de Lisboa,
Lisbon, Portugal

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 APPLIED NEUROPSYCHOLOGY: ADULT, 0: 1–12, 2012
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ISSN: 0908-4282 print=1532-4826 online
DOI: 10.1080/09084282.2012.670145

The Effect of Education on Age-Related Changes in Three

Cognitive Domains: A Cross-Sectional Study in Primary Care
Isabel Pavão Martins, Carolina Maruta, Cláudia Silva, Pedro Rodrigues, Catarina Chester,
Sandra Ginó, Vanda Freitas, and Sara Freitas
Language Research Laboratory, Institute of Molecular Medicine and Faculty of Medicine,
University of Lisbon, Lisbon, Portugal

António Gouveia Oliveira

Department of Biostatistics, Faculty of Medical Sciences,
Downloaded by [Carolina Maruta] at 08:49 23 August 2012

Universidade Nova de Lisboa, Lisbon, Portugal

The present study aims to investigate the protective effect of formal education on
age-related changes in different cognitive domains with the hypothesis that it may
attenuate the rate of decline. Individuals aged 50 years or older attending primary care
physicians without known brain disease (431 participants, mostly [60.3%] female with
66.3 [
9.1] years of age and 7.7 [
4.1] years of education, on average), were evaluated
with a neuropsychological battery including 28 cognitive measures. Cognitive domains
identified by factor analysis were subject to repeated multiple regression analyses to
determine the variance explained by age and education controlling for gender, depress-
ive symptoms, and vascular risk factors. The slope of the regression equation was
compared between two educational groups with an average of 4 years and 11 years
of education, respectively. Factors identified corresponded to processing ability
(Factor 1), memory (Factor 2), and acquired knowledge (Factor 3). Although education
improved performance in Factors 1 and 3, it did not change the slope of age-related
decline in any factor. This study suggests that in culturally heterogeneous groups, small
increments in education enhance cognition but do not modify the rate of decline of
executive functioning with age. These results contradict some clinical findings and need
to be confirmed in longitudinal studies.

Key words: cognitive reserve, education in aging, screening battery

INTRODUCTION performance in spite of the presence of brain pathology

Brain aging is an inevitable consequence of time, yet its
impact in cognition is far from uniform, ranging from
perfect fitness to mental frailty and dementia. This strik-
ing variability can be accounted for, in part, by cognitive
reserve, a construct that explains the ability to maintain
Address correspondence to Isabel Pavão Martins, M.D., Ph.D.,
Language Research Laboratory, Institute of Molecular Medicine and
Faculty of Medicine, University of Lisbon, 1649-028 Lisbon, Portugal.
E-mail: labling@fm.ul.pt
(Park & Reuter-Lorenz, 2009; Stern, 2002, 2006, 2009).
Indeed, several studies have shown that education or
other measures of environmental enrichment may
decrease the rate of conversion to dementia in subjects
with identical degrees of pathological burden of
Alzheimer’s disease (Bennett et al., 2003; EClipSE
Collaborative Members, 2010); may have a protective
role against the cognitive impairment associated to brain
white-matter changes (WMC) or higher ventricular
volume (Brickman et al., 2009; Kuller et al., 1998);
 2 MARTINS ET AL.
may reduce the progression of memory decline and
deterioration both in Alzheimer’s disease (Koepsell
et al., 2008; Le Carret et al., 2005; Stern, Albert, Tang,
& Tsai, 1999) and in vascular dementia (Lane, Paul,
Moser, Fletcher, & Cohen, 2011); may reduce the risk
for dementia during aging (Stern et al., 1994; Valenzuela
& Sachdev, 2006); and may explain cognitive perfor-
mance variability in subjects with WMC (Schmidt et al.,
2011) or with cognitive impairment and dementia
(Vemuri et al., 2011). Those measures, such as reading
ability, vocabulary, mental stimulation, and occupational
attainment, which reflect lifetime experiences, have
therefore been used as surrogate markers of the construct
of cognitive reserve (Jones et al., 2011; Siedlecki et al.,
2009). The number of years of formal education is
probably the most consistently used among them.
Contrasting with this recognized protective effect
upon the consequences of brain disease is the contro-
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versy regarding the role of education on the cognitive
effects of normal aging. The latter has been best charac-
terized by morphometric, functional, and neuropsycho-
logical changes associated with the frontal lobes
(Buckner, 2004), because it is mainly characterized by
a dysfunction of executive abilities like processing speed,
working memory, inhibitory control, top–down sup-
pression (Gazzaley, Cooney, Rissman, & D’Esposito,
2005), or shifting ability. Patterns of functional brain
activation during aging are different from those of
younger adults (Cabeza, Anderson, Locantore, &
McIntosh, 2002; Clapp, Rubens, Sabharwal, &
Gazzaley, 2011) and depend in part on education
(Angel, Fay, Bouazzaoui, Baudouin, & Isingrini, 2010;
Springer, McIntosh, Winocur, & Grady, 2005). Yet,
despite that evidence and the plausibility that lifelong
cognitive stimulation will produce more efficient pat-
terns of functioning and a better ability to develop
new strategies (or scaffolding) to face age-related decline
(Goh & Park, 2009; Satz, Cole, Hardy, & Rassovsky,
2010), previous research has shown that education and
cognitive stimulation do not protect against aging in
all cognitive domains (Batterham, Mackinnon, &
Christensen, 2011; Christensen et al., 1997; Siedlecki
et al., 2009; Tucker & Stern, 2011). Although the
relation between education and age is complex and
variable in different cognitive domains (Ardila,
Ostrosky-Solis, Rosselli, & Gómez, 2000; Capitani,
Barbarotto, & Laiacana, 1996), apparently its protective
effect is much more evident in measures of crystallized
abilities (or ‘‘product’’), like vocabulary, compared
with fluid abilities (or ‘‘processes’’; Christensen et al.;
Salthouse, 2006) like processing speed, memory, or vis-
ual–spatial abilities, which is a paradoxical result taking
into account its more widespread protective effect in
brain pathology. Besides, independently of education,
crystallized measures are more resistant to aging than
are fluid measures, therefore making any protective
effect much more difficult to document. However, some
of the extant studies on that topic used brief and general
measures, did not evaluate systematically different
aspects of cognition (Christensen et al.; Kuller et al.,
1998), focused on cognitive stimulation (Salthouse,
2006) or on late-life decline in individuals older than
70 years of age (Batterham et al.; Christensen, 2001;
Christensen et al.), and did not always control for
vascular risk factors or depressive symptoms that can
also influence cognitive performance (Elias, Elias,
Robbins, & Budge, 2004). Because cognitive decline
may start early in adulthood (Salthouse, 2009) and
affect selective cognitive abilities, long-term memory,
processing speed, reasoning, and spatial ability
(Salthouse, 2004; Christensen), it is important to study
it in large samples of the population, heterogeneous
for age and education with more extensive testing and
controlling for those clinical variables. In addition, it
is not known how ‘‘much’’ difference in education is
necessary to produce a cognitive effect in age-related
decline. A single study estimated the effect of each year
of education on decreasing the risk for Alzheimer’s
disease (Bennett et al., 2003), but most studies address-
ing this matter, performed in North America or with
English-speaking subjects, compared highly performing
subjects (with university background) to those with
lower levels of education, and it is not clear if those
effects also stand in samples with overall lower
education.
The present project (‘‘Mindful Aging: Avoiding
Age-Related Cognitive Decline’’) is a prospective longi-
tudinal study of a cohort of adults followed in primary
care that aims to study cognitive profiles in aging and
to identify the best neuropsychological measures that
predict cognitive decline. The primary care setting of
recruitment was chosen considering that primary care
physicians often miss the early stages of dementia
(Bradford, Kunik, Schulz, Williams, & Singh, 2009),
although this is the most likely place where diagnosis
can be made. This project includes an extensive neuro-
psychological assessment, and analysis of its baseline
results allows us to evaluate the effect of education on
several tests and measures of cognitive performance
across different decades of age, because the study popu-
lation is composed of a rather heterogeneous sample of
individuals of European origin, speaking the same
language and with an identical cultural background,
but who had different degrees of cognitive-intellectual
stimulation, due to different opportunities to access edu-
cation. In addition, most of these individuals have low
levels of education, which is an opportunity to evaluate
the effects of small educational changes.
In this article, we aim to analyze the putative benefit
of education in age-related performance, in different

cognitive domains. Our hypothesis is that: (a) education
will be positively related to current performance in all
age groups and domains, but (b) it will also decrease
age differences in performance (i.e., it may attenuate dif-
ferences across age groups in individuals with higher
education compared with those with lower education,
suggesting, therefore, a modifying role in age-related
cognitive changes). Cognitive aging is measured here
by the average (current) performance obtained by differ-
ent age groups (controlled for gender, vascular risk fac-
tors, depressive symptoms, and living status), and
education is used as a surrogate marker of reserve.
METHODS
Study Design, Research Participants, and Setting
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The present data refer to the baseline cross-sectional
evaluation of a prospective longitudinal cohort study
on aging and cognition of individuals attending prim-
ary care centers in the community. Participants were
recruited from two metropolitan areas belonging to
the National Health Service. All residents of any given
geographic area are entitled to receive health care, and
a single physician (general practitioner [GP]) usually
observes all family members and knows the family
background.
Subjects were screened and invited to participate by
their GP according to the selection criteria: (1) aged 50
years old or older; (2) independence on daily living
based on physician report and self-report; (3) European
Portuguese as their native language; (4) absence of know
brain disease, namely stroke, head trauma with loss of
consciousness, epilepsy, dementia (known or suspected),
psychosis or uncontrolled severe systemic disease (such
FIGURE 1 Flow diagram of participants’ inclusion.
AGING AND EDUCATION 3
as advanced cancer, renal or hepatic failure, or HIV
infection); (5) lack of substance or alcohol abuse; (6)
and willingness and consent to participate. Exclusion
criteria were dementia, mental retardation, or a Mini
Mental State Examination (MMSE; Folstein, Folstein,
& McHugh, 1975) score below education-adjusted cut-
off points, which are 22 for individuals with less than
12 years of education and 27 for those with 12 or more
years of education (Guerreiro et al., 1994; Pedrosa et al.,
2010).
Patients were required to give institutionally appro-
ved informed consent. The study protocol was approved
by the Ethics Committee of Lisbon Faculty of Medicine,
by the institutional boards of participating regional
health centers, and by the National Committee for Data
Protection. Of 544 participants screened, 479 completed
the evaluation. However, because reading is necessary to
perform some of the neuropsychological tests, we only
included in the present analysis individuals with a mini-
mum of 4 years of formal education (corresponding to
the completion of primary school), which means that
48 subjects with very low or no education, who also dif-
fered significantly in age and gender from the other part-
icipants, were excluded from the present study. Other
reasons for exclusion are presented in Figure 1.
Participants’ ages ranged from 50 to 95 years, with an
average of 66 (
9.1) years of age and 7.7 (
4.1) years of
education. The majority were women (60.3%). The
majority (85.6%) were married or lived with some com-
pany, and 14.4% lived alone. The number of years of
formal education did not follow a normal distribution
(Kolmogorov-Smirnov test ¼ 5.1, p < .001); therefore,
participants were divided into two categories: a low edu-
cation group (LE) ranging from 4 to 6 years of formal
education (N ¼ 219) and a higher education (HE) group
with more than 6 years of education (N ¼ 212), which is
 4 MARTINS ET AL.

TABLE 1
Sample Demographic Characteristics, Mean Test Scores, and Standard Deviations on Each Cognitive Measure, by Education Group

Low Education High Education

Variables (4–6 yrs) (>6 yrs) Statistics Differences 95% CI

Age (M
SD) 67.57
8.7 64.45
9.1 T ¼ 3.611 p < .001 ; 1.419, 4.808
Low > High
Education (M
SD) 4.29
0.69 11.19
3.0 T ¼ 32.420 p < .001 ; 7.320, 6.482
Low < High
Gender (F:M) 136:83 124:88 X2 ¼ 0.59 .44;ns —
Hypertension (% yes) 63.4 58.8 X2 ¼ 0.87 .35;ns —
Diabetes (% yes) 16.7 15.8 X2 ¼ 0.06 .82;ns —
High Cholesterol (% yes) 60.9 53.3 X2 ¼ 2.3 .13;ns —
Living Alone (% yes) 15.1 13.7 X2 ¼ 0.17 .68;ns —
MMSE M
SD (min–max) 27.89
1.7 (2230) 29.10
1.1 (2530) T ¼ 8.725 p < .001 ; 1.475, 0.933
Low < High
CVLT-9 Trial 1 (M
SD) 4.82
1.4 5.39
1.2 T ¼ 4.543 p < .001 ; 0.809, 0.321
Low < High
CVLT-9 Trial 5 (M
SD) 7.67
1.3 7.72
1.2 T ¼ 0.424 .672;ns 0.284, 0.184
CVLT-9 Trials 1–5 (M
SD) 33.22
5.5 34.65
4.9 T ¼ 2.837 .005; 2.424, 0.440
Low < High
CVLT-9 SDFR (M
SD) 6.46
1.6 6.82
1.7 T ¼ 2.189 .029; 0.673, 0.036
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Low < High

CVLT-9 SDCR (M
SD) 7.17
1.4 7.46
1.4 T ¼ 2.061 .040; 0.555, 0.013
Low < High
CVLT-9 LDFR (M
SD) 6.62
1.8 6.91
1.7 T ¼ 1.657 .098; ns 0.622, 0.053
CVLT-9 LDCR (M
SD) 7.13
1.6 7.40
1.4 T ¼ 1.846 .066; ns 0.554, 0.017
CVLT-9 Recog. Hits (M
SD) 8.39
1.0 8.50
0.8 T ¼ 1.230 .219; ns 0.291, 0.067
Immediate Visual Reproduction (M
SD) 51.60
18.2 68.09
17.7 T ¼ 9.520 p < .001 ; 19.898, 13.088
Low < High
Delayed Visual Reproduction (M
SD) 28.05
20.2 42.71
23.0 T ¼ 7.012 p < .001 ; 18.770, 10.551
Low < High
WMS-III Faces (M
SD) 31.33
4.4 34.72
4.8 T ¼ 7.608 p < .001 ; 4.272, 2.518
Low < High
Mazes (M
SD) 11.53
6.4 7.27
4.3 T ¼ 8.120 p < .001 ; 3.233, 5.298
Low < High
Trail A (M
SD) 81.26
39.9 51.24
23.8 T ¼ 9.479 p < .001 ; 23.789, 36.244
Low < High
Trail B (M
SD) 208.18
76.3 128.72
63.0 T ¼ 11.685 p < .001 ; 66.099, 92.837
Low < High
Trail B–A difference (M
SD) 128.63
61.3 77.47
50.4 T ¼ 9.378 p < .001 ; 40.434, 61.882
Low < High
Symbol Search (M
SD) 14.70
5.3 22.24
7.2 T ¼ 12.327 p < .001 ; 8.742, 6.337
Low < High
WASI Matrix Reasoning (M
SD) 10.57
4.7 16.77
7.0 T ¼ 10.725 p < .001 ; 7.342, 5.067
Low < High
Stroop Color (M
SD) 47.70
11.5 56.42
12.0 T ¼ 7.624 p < .001 ; 10.966, 6.471
Low < High
Stroop Interference (M
SD) 21.93
8.0 29.06
9.8 T ¼ 8.178 p < .001 ; 8.835, 5.411
Low < High
Stroop Reading (M
SD) 67.03
16.4 82.66
14.8 T ¼ 10.350 p < .001 ; 18.600, 12.663
Low < High
WASI Vocabulary (M
SD) 46.96
11.2 61.47
9.7 T ¼ 14.314 p < .001 ; 16.503, 12.518
Low < High
Information (M
SD) 17.12
2.3 18.82
1.4 T ¼ 9.130 p < .001 ; 2.057, 1.328
Low < High
Category Fluency (Food) (M
SD) 16.60
4.3 19.38
5.0 T ¼ 6.162 p < .001 ; 3.674, 1.897
Low < High
Category Fluency (Animals) (M
SD) 13.85
3.9 18.06
4.7 T ¼ 10.029 p < .001 ; 5.027, 3.380
Low < High
Phonemic Fluency (Letter ‘‘p’’) (M
SD) 7.70
3.9 10.99
4.2 T ¼ 8.361 p < .001 ; 4.062, 2.516
Low < High
Famous Faces Test (M
SD) 22.80
8.6 28.60
7.7 T ¼ 7.284 p < .001 ; 7.358, 4.231
Low < High

(Continued )

TABLE 1
Continued
Low Education
Variables (4–6 yrs)
Digit Span Forward (M
SD) 4.95
1.0
Digit Span Backward (M
SD) 3.37
0.9
SD ¼ standard deviation; CI ¼ Confidence Interval; SDFR ¼ Short-delay free recall; SDCR ¼ Short-delay cued recall; LDFR ¼ Long-delay free
recall; LDCR ¼ Long-delay cued recall; M ¼ mean; WMS-III ¼ Wechsler Memory Scale-Third edition; WASI ¼ Wechsler Abbreviated Scale of
Intelligence; MMSE ¼ Mini-mental state examination; CVLT ¼ 9 ¼ 9-item version of the California Verbal Learning Test; F ¼ female; M ¼ male;
T ¼ t-test; X2 ¼ Chi-square test; ns ¼ not significant at p < .05.

highest level of significance.
in agreement with the organization of the public school
system. Only 14% of the latter had more than 12 years
of education, and just 3% had completed university studies
(17 or 18 years of education). Table 1 displays demo-
graphic and clinical data of the two groups and shows that
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subjects with more education were on average 3 years
younger and had a higher score on the MMSE than those
of LE group. However, they had a similar distribution of
gender, vascular risk factors, and living status.
Construction of the Primary Screening Test Battery
and Neurobehavioral Assessment
The principles underlying the choice of the tests for the
baseline neuropsychological battery were: (1) inter-
nationally recognized tests sensitive to cognitive decline;
(2) ability to evaluate a wide range of cognitive domains,
namely those impaired in Alzheimer’s and vascular
dementia (Chen et al., 2000); (3) ability to detect
age-related changes (Salthouse, 2009), namely speed of
information processing, working memory, and inhibi-
tory control; (4) inclusion of measures resistant to
age-related decline; and (5) ability to administer the bat-
tery in a single visit. The selected battery included 28
cognitive tests or measures, summarized and grouped
by cognitive domain in the Appendix—namely, Symbol
Search (Wechsler, 1997a), Mazes (Porteus, 1959),
Trail-Making Test Parts A and B and B–A (Reitan,
1958), Stroop Test (Stroop, 1935), Vocabulary and
Matrix Reasoning from the Wechsler Abbreviated Scale
of Intelligence (WASI; Wechsler, 1999), Famous Faces
Naming Test (Martins, Loureiro, Rodrigues, & Dias,
2005), Information (Garcia, 1984), a 9-item short ver-
sion of the California Verbal Learning Test (CVLT;
Libon et al., 1996), Digit Span, Faces, and Visual
Reproduction subtests from the Wechsler Memory
Scale-Third Edition (WMS-III; Wechsler, 1997b), and
semantic and phonemic Verbal Fluency tests. Although
many different measures could be obtained from this
battery of tests, we focused on those that are more used
in research and in clinical practice, avoiding overlap
AGING AND EDUCATION 5
High Education
(>6 yrs) Statistics Differences 95% CI

5.61
1.1 T ¼ 6.498 p < .001 ; 0.858, 0.460
Low < High
4.09
1.1 T ¼ 7.160 p < .001 ; 0.923, 0.526
Low < High
between them. However, it is known that some of the
CVLT measures have some correlation among them
(Delis, Kramer, Kaplan, & Ober, 1986).
Participants also undertook a 15-item version of the
Geriatric Depression Scale (GDS; Yesavage et al., 1983)
and questionnaires of subjective memory complaints
(Schmand, Jonker, Geerlings, & Lindeboom, 1997), gen-
eral health (Ware & Sherbourne, 1992), and autonomy in
locomotion and instrumental activities of daily living
(Lawton & Brody, 1969). The latter will not be reported here.
Procedures
Participating GPs performed the first screening of
participants, filled the criteria checklist, and reported
vascular risk factors (hypertension, diabetes and its
type, high serum cholesterol) and current medication.
After informed consent, participants undertook the
MMSE (Folstein et al., 1975). If score was within the
education-adjusted normal range, the participants were
scheduled an evaluation by a licensed psychologist
trained in this battery. Data recorded included demo-
graphic information, current working (retired, emplo-
yed, unemployed), and their living status regarding
present house company (categorized as alone or not
alone), and occupation (present or the longest
occupation in the past). The evaluation took place in a
private office in the local health center.
Data Analysis
Analysis was performed with the Statistical Package for
the Social Sciences Version 19.0. To identify the cogni-
tive domains underlying the 28 tests and measures, with-
out an a-priori assumption, their raw scores were
submitted to an exploratory factor analysis with vari-
max rotation accepting eigenvalues superior to 1 accord-
ing to the scree plot. Identified factors were transformed
into variables, each corresponding to the average stan-
dard scores of tests loading on that factor. Therefore,
each variable was a composite measure of each cognitive
 6 MARTINS ET AL.

domain. To investigate the effect of education and
age on each domain, we conducted multiple linear
regression analyses adjusted by gender, presence of
any vascular risk factor, depressive symptoms (defined
by 3 or more points on the GDS), and living status
(alone=not alone). Due to the multiplicity of tests, and
considering the exploratory nature of this study, results
were considered statistically significant at p < .01.
RESULTS
The 28 measures presented in the Appendix were included
in an exploratory factor analysis. The scree plot suggested
that maximum variance was explained by three factors,
and this solution explained 53.9% of the variance. The
rotated component matrix is presented in Table 2.
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Factor 1 (F1) is composed of tests of attention,
processing speed, inhibitory control, switching and
abstract reasoning, and visual or visuomotor memory
and was designated ‘‘processing ability.’’ Factor 2
(F2), ‘‘memory,’’ includes all subtests and measures of
the CVLT. Factor 3 (F3) is composed of verbal (seman-
tic and phonemic) fluency tasks, vocabulary, informa-
tion, famous faces, and digit spans and is designated
‘‘acquired knowledge.’’
Mean scores and standard deviations obtained in
each test, by education group, are presented in Table 1.
A mean standard score was computed from the standard
scores of tests loading in each factor. Those were subject
to regression analysis (dependent variable) to analyze
the effect of demographic (age, education, and gender),
clinical (significant depressive symptoms or not and
presence or absence of vascular risk factors), and living
status (living alone or not) on those domains (Table 3).

TABLE 2 A dichotomic division of depressive symptoms was used

Exploratory Factor Analysis With a Principal Component Analysis instead of the GDS score because the latter did not
and Varimax Rotation
present a normal distribution (Kolmogorov-Smirnov
Factor 1 Factor 3 Z ¼ 3.843, p < .000). Apart from that, this scale had a
(Processing Factor 2 (Acquired
Items Ability) (Memory) Knowledge) TABLE 3
Influence of Education, Age, Gender, Depression, Vascular Risk
CVLT-9 Trial 1 .137 .541 .224
Factors, and Living Status on Cognitive Performance
CVLT-9 Trial 5 .185 .764 .010
CVLT-9 Trials 1–5 .232 .820 .093 Adjusted
CVLT-9 SDFR .169 .850 .021 R2 Beta t p 95% CI
CVLT-9 SDCR .114 .853 .076
CVLT-9 LDFR .083 .871 .110 Processing .407
CVLT-9 LDCR .073 .890 .097 Ability (F1)
CVLT-9 Recog. hits .001 .523 .066 Age .499 11.543 <.001 0.066, 0.047
Immediate Visual .690 .223 .184 Education .319 7.708 <.001 0.473, 0.796
Reproduction Gender .086 2.014 .045 0.344, 0.004
Delayed Visual Reproduction .634 .281 .096 Depression .144 3.422 .001 0.472, 0.127
WMS-III Faces .399 .236 .184 Vascular risk .010 0.241 .810 0.175, 0.224
Mazes .510 .035 .396 factors
Trail A .625 .028 .426 Living status .035 0.821 .412 0.143, 0.347
Trail B .711 .069 .481 Memory (F2) .201
Trail B–A difference .579 .075 .389 Age .156 3.108 .002 0.029, 0.007
Symbol Search .781 .101 .323 Education .010 0.204 .839 0.211, 0.172
WASI Matrix Reasoning .519 .132 .397 Gender .416 8.415 <.001 0.658, 1.060
Stroop Color .650 .171 .306 Depression .037 0.765 .444 0.283, 0.124
Stroop Interference .741 .173 .167 Vascular risk .050 1.028 .304 0.112, 0.359
Stroop Reading .434 .057 .502 factors
WASI Vocabulary .272 .134 .719 Living status .013 0.260 .795 0.328, 0.251
Information .172 .004 .666 Acquired .216
Category Fluency (Food) .234 .269 .551 knowledge
Category Fluency (Animals) .301 .158 .680 (F3)
Phonemic Fluency (Letter ‘‘p’’) .234 .111 .695 Age .066 1.327 .185 0.019, 0.004
Famous Faces Test .199 .231 .597 Education .436 9.162 <.001 0.681, 1.053
Digit Span Forward .302 .096 .455 Gender .127 2.583 .010 0.452, 0.061
Digit Span Backward .387 .051 .433 Depression .066 1.375 .170 0.060, 0.336
Eigenvalue 9.777 4.068 1.252 Vascular risk .016 0.344 .731 0.189, 0.269
% Cumulative Variance 34.9 49.4 53.9 factors
Living status .056 1.168 .244 0.449, 0.114
CVLT-9 ¼ 9-item version of the California Verbal Learning Test;
SDFR ¼ Short-delay free recall; SDCR ¼ Short-delay cued recall; Note: Regression analysis: Factor 1 was positively associated with
LDFR ¼ Long-delay free recall; LDCR ¼ Long-delay cued recall; educational level but negatively associated with age and depression.
WMS-III ¼ Weschler Memory Scale-Third Edition; WASI ¼ Weschler Factor 2 was associated with female gender but negatively associated
Weschler Abbreviated Scale of Intelligence. with age. Factor 3 was positively associated with education level.

good internal consistency (Cronbach’s alpha ¼ .834),
presented a negative correlation with education level
(Spearman’s rho ¼ .22, p < .000), had a higher score
among females compared with males (Mann-Whitney
U Test, p < .000), and had no significant correlation
with age (rho ¼ .06, p ¼ .192, ns).
Multiple regression analysis showed that after adjust-
ment by vascular risk factors and depression, F1 was
significantly and positively associated with educational
level (p < .001) and was negatively associated with age
(p < .001) and depression (p ¼ .001). F2 was negatively
associated with age (p ¼ .002) and female gender
(p < .001) but not with educational level (p ¼ .84). F3
was positively associated with education level (p < .001)
but not with age (p ¼ .19). To evaluate the effect of
education on age-related changes, the slope of the
decline was compared between the two main educational
groups by testing the significance of a term representing
Downloaded by [Carolina Maruta] at 08:49 23 August 2012
the interaction of age  education. The interaction of
age  education was not statistically significant for any
of the three factors: F1 (beta ¼ .497, ns), F2 (beta ¼
.251, ns), and F3 (beta ¼ .371, ns).
DISCUSSION
This study analyzed the effect of education on age-
related cognitive performance, in nondemented adults
with a heterogeneous cultural background followed in
FIGURE 2 Performance on the three cognitive factors by age and education groups. Z scores obtained in the three cognitive measures identified by
factor analysis are displayed by age in decades and education: (A) Processing Ability (F1; top); (B) Memory (F2; middle); and (C) Acquired Knowl-
edge (F3; bottom). Solid line ¼ Lower Education (4–6 years); dashed line ¼ higher education (>6 years).
AGING AND EDUCATION 7
primary care through a comprehensive battery of tests.
The two study groups had an average difference of 7
years in education, but most individuals in the HE
group did not have a university background, which
makes this a comparison between minimum and
medium educational background, thus different from
most previous studies.
Factor analysis yielded three main factors. F1 is com-
posed of most tests aimed to evaluate executive abilities
but also visuospatial processing, an identical factor
loading (executive and visuospatial) of other batteries
(Pontón, Gonzalez, Hernandez, Herrera, & Higareda,
2000). F2 congregates the different dimensions of verbal
episodic memory, learning, retrieval, and recognition,
and F3 includes measures of acquired and consolidated
rote verbal knowledge (crystallized measures) as well as
the digit span tests, possibly because they require rote
verbal knowledge. Overall, this factor structure is in
agreement with the domains those tests were expected
to evaluate, thus providing a measure of construct val-
idity of the selected battery. The small percentage of
variance explained by this factor solution suggests that
other variables also contribute to the variance observed
in this battery of tests.
Regression analysis showed that education and age
had different effects on each cognitive domain. The
‘‘acquired knowledge’’ factor, as expected, was very
closely related to education but did not significantly
decrease with age or vascular risk factors, corroborating
 8 MARTINS ET AL.
the findings of other studies showing that knowledge-
based verbal abilities are less vulnerable to aging or
vascular variables (Babcock & Salthouse, 1990; Elias
et al., 2004; McArdle, Ferrer-Caja, Hamagami, &
Woodcock, 2002; Salthouse, 2004; Tucker-Drob, 2011)
but are closely related to the information acquired
during life. From the observation of Figure 2, it is
apparent that this cognitive domain declines late in life,
and therefore, it might be an inadequate compound
measure to investigate age-related changes in a span of
four decades. In fact, studies that demonstrated a pro-
tective effect of education on crystallized measures were
performed in the eldest range of the population, as part
of studies of terminal decline (Batterham et al., 2011).
The ‘‘memory factor,’’ on the contrary, declined
significantly with age, starting apparently at (or possibly
before) the age of inception. Female gender had a signifi-
cant and positive effect on this domain, as women are
Downloaded by [Carolina Maruta] at 08:49 23 August 2012
known to have a better performance on tests of verbal
memory compared with men, from an early age (Martins,
Castro-Caldas, et al., 2005). However, education did
not have a significant effect on this factor. This was
also found in other cohorts (Ardila et al., 2000) but
contradicts findings showing that education may delay
the speed of memory decline (Manly, Touradji, Tang,
& Stern, 2003). This lack of effect can have different
explanations. Firstly, the measure used is a compound
score that includes learning and delayed recall but also
tests like word recognition that tackle ‘‘familiarity,’’ a
distinct cognitive process within memory. Secondly,
the short version of the CVLT is relatively easy just
like the memory test used by Ardila et al. and might
be less sensible to education (Norman, Evans, Miller,
& Heaton, 2000). Thirdly, some authors (Salthouse,
2004, 2009) postulate that memory decline begins ear-
lier than the inception age of this study, and therefore,
the main difference might be attenuated at this stage.
The processing factor score, on the other hand,
showed a significant and positive effect of education
but a negative effect of age and depressive symptoms.
This is in agreement with previous studies (Clark,
Chamberlain, & Sahakian, 2009) and supports the
theory that normal aging corresponds mainly to a
decline in executive functions (Salthouse, 1996), in
addition to long-term declarative memory. However,
the hypothesis that education could modify the course
of age-related decline was not supported, at least in what
concerns executive abilities.
In summary, the pattern of age-related performance
found in this analysis corroborates the evidence that
age-related decline varies as a function of cognitive
domain and is enhanced by less education (Brickman
et al., 2009; Park & Reuter-Lorenz, 2009; Vemuri et al.,
2011), even among subjects with an overall low edu-
cational level. Yet, contrary to what was found by other
authors (Ardila et al., 2000; Capitani et al., 1996), the
effect of education was mostly of a cognitive enhancer,
expressed by a higher performance at all ages, but it
did not modify the slope of the regression line represent-
ing age-related decline. This result suggests that indivi-
duals with higher and longstanding cognitive activity
(indirectly measured by the number of years of edu-
cation) tend to mitigate decline. They will maintain a
better level of performance over the years compared
with those with lower education, at least from 50 years
onward. However, their age-related change in cognition
proceeds at an identical pace. This is intriguing given the
fact that education protects or may modify decline asso-
ciated with pathological burdens (Manly et al., 2003).
We acknowledge several limitations to this study.
Firstly, it is a cross-sectional study where decline is
determined as a comparison between current age-group
performance and not as individual decline over time.
Secondly, the criteria to exclude dementia consisted
mainly in clinical information provided by the GP and
the MMSE score, which may lack sensitivity. Thirdly,
it does not include genetic, imaging, or other biological
markers that are known to be associated with decline.
This is particularly relevant when we are studying cogni-
tive reserve, for they may provide markers of patholo-
gies. However, these are not easy to obtain in large
samples of healthy individuals. In addition, we could
not include subjects with the lowest formal education
in the comparison, nor were we able to include a homo-
geneous sample of subjects with the highest education
who could represent the extreme range of this variable,
which limits the conclusions from the data. Due to
changes in educational policies during the last decades,
the minimum level of compulsory education has
increased, and it is now difficult to encounter young,
healthy individuals with low levels of education. How-
ever, the analysis with the full sample of 479 subjects
reproduced exactly the same results, despite the fact that
illiterate participants could not perform some of the
tests requiring reading or paper-and-pencil practice.
Finally, some of the tests were not applied in the full
version (only some subtests were used) or were just
translated to Portuguese (Vocabulary and CVLT items).
With these limitations, we consider these results prelimi-
nary, and further research is needed through longitudi-
nal studies. We also recognize that despite extensive
testing we decided to compare composite measures,
representing general domains to include all cognitive
data collected. It is possible that individual tests directed
to more selective areas could produce a different magni-
tude of decline in this age span and could be more
adequate for evaluating the effect of education on
age-related changes.
We considered the level of education attained as the
best surrogate marker of cognitive reserve. However,

we acknowledge that this is a complex measure because
education early in life modifies cognitive stimulation
irreversibly and contributes to the opportunity of attain-
ing cognitively challenging vocations and avocations,
leading to a lifelong amplification of its effect upon cog-
nition. At the time these participants attended school,
some 45 to 70 years ago, it was common for children
not to attend school or to complete only the 1st years
of primary school and to begin to work very early in life
to contribute to the family support. This was not due to
lack of intelligence or skills but to poverty and perhaps
to lack of recognition of the power of education, leading
together to a lack of opportunity. Of course, poverty is
associated with low socioeconomic status, poor diet, and
less preventive health measures, which may have conse-
quences on brain development and general health. Yet,
those variables are difficult to evaluate retrospectively.
Education, as it is used here, is probably a very general
Downloaded by [Carolina Maruta] at 08:49 23 August 2012
measure of all those influences.
The strengths of this analysis are the extensive testing,
controlling for clinical factors that influence cognition
(vascular risk factors and depressive symptoms), and
the education interval studied, which is unusual and repli-
cated some results for narrow educational differences.
In conclusion, this study corroborates the positive influ-
ence of epigenetic factors in aging in some cognitive
domains, even for small differences in educational level,
but it does not support that they delay or modify
age-related changes, at least for this magnitude of edu-
cational range (Dotson, Beydoun, & Zonderman, 2010).
It underlines the need to understand how cognitive stimu-
lation changes brain and cognition as a first step to develop
preventive strategies for cognitive decline and dementia.
ACKNOWLEDGEMENTS
The authors thank Fundação Calouste Gulbenkian for
sponsoring the present study (Project 0488). The authors
are indebted to all participants and to GPs and Health
Center Directors who collaborated in this study, namely
Drs. Teresa Costa, Teresa Mota, Elisabete da Fonseca,
Luı́s Afonso, Renato Graça, Cristina Galamba, Helena
Febra (Centro de Saúde da Lapa); Cecı́lia Cabral, Eugé-
nio Oliveira, Paula Freitas, Neto Nogueira, Edite
Branco, Helena Ferreira (Centro de Saúde de Alcântara);
Luı́sa Romeiro, Rosário Braz, Teresa Libório, Óscar
Miranda, Teresa Campos, Áurea Farinha, Isabel
Santos, Nave Ferreira, Cristina Bastos, Rita Lourenço,
Judite Viana, Manuel Rosmaninho, Luı́sa Costa, Isabel
Santos, Bernardino Costa, Luı́sa Teixeira (Centro de
Saúde de Oeiras); Elisabete Serra, João Reis, Maria José
Heleno, Rui Cóias, Maria João Mendes, Sónia Pereira,
Carla Coimbra (Centro de Saúde de Paço D’Arcos); Ana
Paula Granadeiro, Rosa Oliveira, Analila Cruz, Vı́tor
AGING AND EDUCATION 9
Cardoso (Centro de Saúde Moita); João Belbut,
Manuela Ribeiro, José Luı́s Gomes, Susete Gomes,
Maria José Rosa (Centro de Saúde do Barreiro); Jaime
Torre, Miguel Santos, Luı́s Pinto, Paula Dias, Raquel
Caetano (Centro de Saúde do Lavradio); Manuela Cruz
(Centro de Saúde de Benfica); Graça Carneiro, Ana
Maria Ferreira, Pedro Silva, Elvira Nunes, Paula
Atalaia (Centro de Saúde de Alvalade); Maria José
Galha, Emı́lia Soares, Rosário Martins, Rogério Costa,
Paula Costa, Teresa Neto, João Costa, Vitória Amaral,
Carmo Velez, Luı́sa Santana (Centro de Saúde de
Évora); and Fátima Portugal, Maria João Palma, Maria
José Luı́s (Centro de Saúde de Sete Rios).
The authors also thank Profs. Maria Amália Silveira
Botelho and Manuela Guerreiro and Dr. Sofia
Madureira for their contribution in the discussion and
organization of the evaluation battery.
Initial concepts and framework developed by Isabel
Pavão Martins. Acquisition of subjects and data by
Carolina Maruta, Claudia Silva, Pedro Rodrigues,
Catarina Chester, Sandra Ginó, Vanda Freitas, and Sara
Freitas. Data analysis and interpretation by António
Gouveia de Oliveira, Isabel Pavão Martins, and Carolina
Maruta. Preparation of manuscript by Isabel Pavão Mar-
tins, Carolina Maruta, and António Gouveia.
The sponsor (Fundação Calouste Gulbenkian) had
no participation in any of the scientific steps of the study
or in writing the article.
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 12 MARTINS ET AL.

APPENDIX

List of Cognitive Tests by Domain Evaluated

Domain Evaluated

Attention Episodic Inhibitory

and Memory Control
Processing Semantic and Visuospatial and Abstract
Test References Speed Language Memory Learning Perception Shifting Reasoning

Symbol Search Wechsler, 1997a þ þ

Mazes Porteus, 1959 þ þ
Trail A Reitan,1958 þ þ
Trail B þ þ þ
Trail difference (B–A) þ
Stroop Reading Stroop, 1935 þ þ
Stroop Color Naming þ
Stroop Interference þ
WASI Vocabulary Wechsler, 1997b þ þ
Downloaded by [Carolina Maruta] at 08:49 23 August 2012

WASI Matrix Reasoning þ þ

Famous Faces Naming Test Martins, Loureiro, et al., þ þ
2005
Information Garcia, 1984 þ þ
CVLT-9 Trial 1 Libon et al., 1996 þ
CVLT-9 Trial 5 þ
CVLT-9 Trials 1–5 þ
CVLT-9 SDFR þ
CVLT-9 SDCR þ
CVLT-9 LDFR þ
CVLT-9 Recog. þ
WMS-III Faces Wechsler, 1999 þ þ þ
WMS-III Visual þ þ þ
Reproduction
Digit Span þ þ
Verbal Fluency (Food= þ þ
Animals;
Letter ‘‘p’’)

CVLT ¼ California Verbal Learning Test 9-item version; SDFR ¼ Short-Delay Free Recall; SDCR ¼ Short-Delay Cued Recall; LDFR ¼
Long-Delay Free Recall; WASI ¼ Wechsler Abbreviated Scale of Intelligence; WMS–III ¼ Wechsler Memory Scale-Third Edition.