Braz J Psychiatry. 2020 May-Jun;42(3):286-294
doi:10.1590/1516-4446-2019-0539
Brazilian Psychiatric Association
0 0 0 0 -0 02-7316-1 85
ORIGINAL ARTICLE
Brazilian version of the European Cross-Cultural
Neuropsychological Test Battery (CNTB-BR):
diagnostic accuracy across schooling levels
Narahyana B. Araujo,10 0 -0 0 -0 0 -0 0 Thomas R. Nielsen,2 Maria L. Barca,3,4 Knut Engedal,3,4
Valeska Marinho,1 Andrea C. Deslandes,1 Evandro S. Coutinho,5 Jerson Laks1,6
1
Instituto de Psiquiatria (IPUB), Universidade Federal do Rio de Janeiro (UFRJ), Rio de Janeiro, RJ, Brazil. 2Danish Dementia Research
Centre, University of Copenhagen, Copenhagen, Denmark. 3Norwegian National Unit for Aging and Health, Vestfold County Hospital,
Toensberg, Norway. 4Department of Geriatric Medicine, Oslo University Hospital, Norway. 5Escola Nacional de Saúde Pública (ENSP),
Fundac¸ão Oswaldo Cruz (FIOCRUZ), Rio de Janeiro, RJ, Brazil. 6Programa de Pós-Graduac¸ão em Biomedicina Translacional (Biotrans),
Universidade do Grande Rio (Unigranrio), Duque de Caxias, RJ, Brazil.
Objective: To translate, establish the diagnostic accuracy, and standardize the Brazilian Portuguese
version of the European Cross-Cultural Neuropsychological Test Battery (CNTB) considering schooling
level.
Methods: We first completed an English-Brazilian Portuguese translation and back-translation of the
CNTB. A total of 135 subjects aged over 60 years – 65 cognitively healthy (mean 72.83, SD = 7.71;
mean education 9.42, SD = 7.69; illiterate = 25.8%) and 70 with Alzheimer’s disease (AD) (mean
78.87, SD = 7.09; mean education 7.62, SD = 5.13; illiterate = 10%) – completed an interview and
were screened for depression. The receiver operating characteristic (ROC) analysis was used to verify
the accuracy of each CNTB test to separate AD from healthy controls in participants with low levels of
education (p 4 years of schooling) and high levels of education (X 8 years of schooling). The optimal
cutoff score was determined for each test.
Results: The Recall of Pictures Test (RPT)-delayed recall and the Enhanced Cued Recall (ECR) had
the highest power to separate AD from controls. The tests with the least impact from schooling were
the Rowland Universal Dementia Assessment Scale (RUDAS), supermarket fluency, RPT naming,
delayed recall and recognition, and ECR.
Conclusions: The Brazilian Portuguese version of the CNTB was well comprehended by the
participants. The cognitive tests that best discriminated patients with AD from controls in lower
and higher schooling participants were RPT delayed recall and ECR, both of which evaluate
memory.
Keywords: Alzheimer’s disease; education; psychometric tests; diagnostic accuracy
Introduction
Nearly 17% of the world’s adult population is illiterate.1
Among older adults, illiteracy and low levels of education
are more common in lower and middle income countries
than in developed countries1 – data from 105 less developed countries for which information is available show
that 43% of the population aged 60 or older were illiterate
in 2010. In some developed countries, however, the
illiteracy rates are also high in old adults.1
Brazil, the country with both the largest territory and
population in South America, is no exception – the country
faces low levels of education, currently associated with
an exponential growth in the population of older adults.
According to data from the Brazilian Institute of Geography
Correspondence: Narahyana B. Araujo, Rua Conde de Bonfim,
1357/504, Tijuca, CEP 20530-001, Rio de Janeiro, RJ, Brazil.
E-mail: narahyana@hotmail.com
Submitted May 03 2019, accepted Oct 14 2019, Epub Feb 21 2020.
and Statistics (Instituto Brasileiro de Geografia e Estatı́stica [IBGE]), 23% of the nearly 29.9 million people above
age 60 years are illiterate in Brazil.2 Nevertheless, few
validated instruments are available in Brazilian Portuguese
for cognitive assessment of people with less than 9 years
of education.3,4
Several publications in Brazil have investigated the
impact of education on the subject’s performance in
cognitive testing. Cognitive batteries for the detection of
mild dementia, such as the Mini Mental State Examination
(MMSE),3 Addenbrooke’s Cognitive Examination-Revised
(ACE-R),5 and Montreal Cognitive Assessment (MoCA),6
have shown a significant correlation between the total
test score and education. The influence of education on
performance has also been evaluated in the Cambridge
How to cite this article: Araujo NB, Nielsen TR, Barca ML, Engedal
K, Marinho V, Deslandes AC, et al. Brazilian version of the European
Cross-Cultural Neuropsychological Test Battery (CNTB-BR): diagnostic accuracy across schooling levels. Braz J Psychiatry. 2020;
42:286-294. http://dx.doi.org/10.1590/1516-4446-2019-0539
Diagnostic accuracy of CNTB-BR
Cognitive Examination (CAMCOG),7-9 the Alzheimer’s
Disease Assessment Scale cognitive subscale (ADASCog),10 and the Consortium to Establish a Registry for
Alzheimer’s Disease (CERAD).11
More recently, the Danish Dementia Research Center
designed the European Cross-Cultural Neuropsychological Test Battery (CNTB) – a battery of tests to assess
cognitive impairment in dementia disorders across ethnic
groups and in people with limited or no education.12 The
CNTB provides scales that are less influenced by linguistic, cultural, and educational factors12 with crosscultural diagnostic properties that are useful for evaluating
dementia in minority populations. Thus, the CNTB, developed to minimize the influence of culture, language, and
educational level,13 may represent a valid alternative to
other neuropsychological batteries.14
Our group has recently validated a Brazilian Portuguese
version of the Rowland Universal Dementia Assessment
Scale (RUDAS),15 showing that it is accurate and valid
to assess neuropsychological performance regardless of
the person’s educational level. However, the availability of
methods for accurate assessment of multidomain cognitive
functioning in illiterate and older adults with low levels of
education is becoming increasingly important in Brazil. In
order to bridge this gap, we aimed to translate, verify the
diagnostic accuracy, and standardize the Brazilian Portuguese version of the CNTB considering educational level.
Methods
Participants
287
diseases, who were cognitively healthy according to clinical evaluation and MMSE. The cutoff used was 13 points
for illiterate participants, 18 points for those with elementary or middle schooling (o 8 years), and 26 points for
those with schooling (X 8 years).19 Neurological or psychiatric diseases were evaluated during the clinical assessment. Imaging and laboratory evaluations were required
of all patients.
All participants regular patients at the aging research
center, private hospital, military hospital or university
center, and had been diagnosed with AD or confirmed as
cognitively healthy. They were evaluated again before
being referred to this study according to the inclusion and
exclusion criteria. Because all those referred agreed to
participants, all participants were included in the final
sample of this study.
The low levels of schooling group included illiterate
participants with up to 4 years of schooling. The high
levels of schooling group included participants with 8 or
more years of schooling.
Procedures
This study was conducted from 2014 to 2017. All
participants completed a session lasting approximately
90 minutes, including a structured demographic and
medical interview, as well as screening for depression
with the Geriatric Depression Scale (GDS-15)20 and the
CNTB.
Measures
15
Detailed data about participants are provided elsewhere.
In summary, participants were selected if they met the
inclusion criterion of at least 60 years of age. Participants
with and without dementia due to Alzheimer’s disease (AD)
were included. Exclusion criteria included neurological
comorbidities, psychiatric clinical disorders, and visual or
hearing impairment that precluded cognitive testing. Subjects with depressive symptoms who did not fulfill clinical
criteria for a depressive disorder were not excluded.
Patients with AD were recruited from a university center
and a military hospital. Clinical diagnosis of AD according
to the DSM-IV16 and the National Institute of Neurological
and Communicative Diseases and Stroke/Alzheimer’s
Disease and Related Disorders Association (NINCDSADRDA)17 was required, with mild or moderate severity
according to the Clinical Dementia Rating (CDR).18 The
diagnostic workup for AD patients included complete blood
cell count, platelet count, glycemia, triglycerides, total
cholesterol and fractions, alkaline phosphatase, glutamic
oxaloacetic transaminase and glutamic pyruvic transaminase, bilirubins, urea, creatinine, total proteins, calcium,
free T4 levels, thyroid-stimulating hormone (TSH) levels,
venereal disease research laboratory (VDRL) test, and
dosage of B12 and folates. Cranial computed tomography
scan or magnetic resonance imaging scan with or without
spectroscopy were also performed.
The control group was recruited from a research center
on aging, a private hospital, and a military hospital, and
included individuals without neurological or psychiatric
Demographic and medical interview
The interview consisted of questions about demographic
data (age, sex, marital status, schooling in years), physical and mental health status, and self-perceived general
health and memory.
Geriatric Depression Scale (GDS-15)
The GDS-15 is a self-report instrument with a dichotomous
response format (yes/no), commonly used for clinical work
and research. The 15-item version was used in this study.
The cutoff used was 6 points.20
European Cross-Cultural Neuropsychological Test Battery
(CNTB)
The CNTB covers the cognitive domains of global cognitive function: memory, language, executive functions, and
visuospatial functions. Only the RUDAS included printed
instructions that required translation and back-translation;
a Brazilian Portuguese version validated by Araujo et al.15
was used. All other tests were based on oral rather than
printed instructions and presented in pictures rather than
verbal stimuli.12
The experimental version of the CNTB was tested for
comprehensibility in four subjects: two healthy older adults
(one with p 4 years of schooling and one with X 8 years of
schooling) and two older adults with AD (one with p 4
years of schooling and one with X 8 years of schooling).
Braz J Psychiatry. 2020;42(3)
288
NB Araujo et al.
Based on this pilot study, it was determined that the CNTB
demonstrated adequate comprehensibility and no changes
to the original items of the CNTB were necessary.
Global cognitive function
RUDAS is a brief cognitive instrument that contains six
items, testing memory (registration and recall), body orientation, praxis, drawing, judgment, and language, adding
up to a total score of 30. Lower scores indicate poorer
cognitive function.21
Memory
The Recall of Pictures Test (RPT) was developed to
assess immediate and delayed recall. The test is similar
to a test from the Brief Cognitive Screening Battery
(BCSB),22 except that color pictures are used. Subjects
are required to learn and recall 10 different pictures. Participants were shown a sheet with 10 pictures of common
objects that had to be named, and immediately thereafter
recalled by the subjects (incidental recall). The pictures
were shown for 30 seconds two additional times and
participants were asked to memorize and recall the
objects (immediate recall). After a 10-minute interference
interval, in which subjects performed other tests, delayed
recall of the objects in the pictures was requested,
followed by a recognition trial in which the 10 pictures
had to be recognized among 10 distracters.12,23,24
In the Enhanced Cued Recall (ECR), 16 pictures are
shown, divided into four cards. When the cards are presented, a semantic cue is given for each picture, and the
participant is asked to identify the picture on the card that
best fits with the cue. Then, an immediate recall of the
four pictures is tested with the same semantic cue for
each picture. After presentation of all four cards, participants are required to name the month backward or
count backward from 20, immediately followed by a free
and cued recall trial. Total score of free and cued recall is
used with a range of scores of 0-16 points.12
A semicomplex figure is also given, consisting of
11 elements. Participants are required to copy and recall
the figure after a 3-minute interference interval.12 This is
scored according to the Meyers & Meyers,25 with a score
range of 0-22 points.
Language
Picture naming including the number of pictures correctly
named at the initial presentation of the colored pictures of
common objects in the RPT was recorded, for a score
ranging from 0-10 points.12
Animal verbal fluency (VF) is a 1-minute assessment in
which participants are asked to name as many animals as
they remember.26,27 Repeated words are not counted
towards the final score.
Supermarket fluency (SF) is a 1-minute test in which
subjects are required to generate as many different
‘‘things you can buy in a supermarket’’ as possible. The
score is equivalent to the number of items produced in
1 minute.12,23,24
Braz J Psychiatry. 2020;42(3)
Executive functions
The Color Trails Test (CTT) is similar to Trail Making Test
(TMT).27 The test has two parts: in CTT 1, participants are
required to connect numbered circles in ascending order,
and in CTT 2, participants are required to switch between
the pink and yellow colors while connecting circles in an
ascending sequence.12,28 The CTT 2 was applied only to
participants with 5 years or more of schooling.
The Five Digit Test (FDT)29 is similar to Stroop Color
test, but designed to minimize the need for schooling.
Participants are exposed to four conditions: 1) naming
a series of 50 digits; 2) counting a series of 50 asterisks;
3) counting a series of 50 digits in which the numeric
value of the digits is incongruent with the number of digits;
and 4) switching between counting and naming incongruent digits. The score is the time in seconds required to
complete each condition in the test.30
Serial threes is similar to the serial sevens subtest from
the MMSE. Participants are required to count down from
20 by threes.12
Visuospatial functions
In copying of simple figures, participants are required
to copy a cross and a four-pointed star according to a
0-3 point scale with a total copying score of 0-6 points.12
The Clock Drawing Test (CDT) was administered using
a pre-drawn circle. Participants are required to add numbers and indicate the time 11:10. The CDT was scored
according to the Shulman criteria (0-5 points).31
In the Clock Reading Test (CRT), the subjects were
required to read the time on a series of 12 clocks showing
different times. The clocks had no digits around the dial.
One point was given for each correct reading and to a
reading less than 4 minutes off the correct time. A half
point was given to readings that were 4 to 5 minutes or
exactly 1 hour off the correct time. The total score was the
sum of the 12 clock readings.12,23,24
Statistical analysis
Descriptive statistics were calculated for demographic
and medical characteristics of the groups. Participants
were divided into an AD and a control group according
to schooling levels – low schooling (p 4 years) or high
schooling (X 8 years).
Receiver operating characteristic (ROC) curve analysis
was used to verify the accuracy of each CNTB test to
detect cognitive impairment in AD. Sensitivity, specificity,
positive likelihood ratio (LR+), and negative LR (LR-)
were calculated. The LR+ was calculated as the ratio
between the proportion of true-positives and the proportion of false-positives. The LR- was obtained by dividing
the proportion of false-negatives by the proportion of truenegatives. Values greater than 1 are desirable for LR+,
and values lower than 0 are appropriate for LR-. The
optimal cutoff score was determined for each test by
balancing sensitivity and specificity according to Youden
index score. Differences with p-values p 0.05 were
considered statistically significant.
All analyses were conducted using Stata14.
Diagnostic accuracy of CNTB-BR
Ethics statement
This study was approved by the ethics committee of the
Instituto de Psiquiatria, Universidade Federal do Rio de
Janeiro, and of the Hospital Naval Marcı́lio Dias, Brazil,
and all participants provided written informed consent
before any procedure took place.
Results
The final sample included 135 older adults (age X 60
years), of which 70 had AD. Table 1 shows clinical and
sociodemographic data. Patients in the AD group were
significantly older, but there was no statistically significant
difference in schooling between the groups. In the control
group, 25.8% were illiterate, and in the AD group, 10%
were illiterate. While most participants in the control group
were widowed, most participants in the AD group were
married. Also, most participants in both groups considered
289
their overall health as good and considered their memory
as ‘‘fairly good.’’ In the AD group, 80% of the sample had
mild AD.
Partial results from the RUDAS-BR study have been
presented in a previous publication.15 For the present
study, results appear in Tables 2, 3 and 4.
In SF, RPT-picture naming, RPT-delayed recall, and
ECR, there is little variation in the optimal cutoff between
the different educational levels. The diagnostic accuracy
of these tests, i.e., the ability to correctly classify cognitive
impairment in AD, did not significantly differ between
the low and high schooling groups. The results show
lower impact of education on these scales, which is very
important for cognitive evaluation in elderly multicultural
patient populations with different educational levels.
Conversely, the optimal cutoff for diagnostic accuracy
using the VF, CTT1, FDT, CDT, CRT, and copying of
simple figures, i.e., tests that evaluate executive function
and visuoconstruction ability, does substantially vary due
Table 1 Sociodemographic and clinical characteristics of the sample
Control (n=65)
AD (n=70)
p-value
72.8367.71
90.77
78.8767.09
56.34
o 0.001
o 0.001*
37
31
32
8
59
33
9.4267.69
25.8
7.6265.13
10
Self-reported health
Very bad
Bad
Fair
Good
Very good
1.50
9.20
36.90
41.50
10.80
1.40
2.80
33.80
53.50
8.50
Self-reported memory
Very bad
Bad
Fair
Good
Very good
0
1.30
44.60
35.40
7.70
5.60
22.50
46.50
23.90
1.40
100
0
0
0
80
20
Diabetes
Hypertension
Depression
20.00
52.31
15.38
30.43
52.17
27.54
Smoking status
Never smoked
Ex-smoker
Current smoker
59.40
37.50
3.10
41.40
52.90
5.70
0
2.5262.56
4.29
2.5862.98
Age in years, mean 6 SD
Female sex
Marital status
Single/divorced
Married
Widower
Schooling in years, mean 6 SD
Illiterate
CDR
0
1
2
Alcohol use
GDS-15 score, mean 6 SD
o 0.001*
0.109
o 0.001*
0.45*
0.04*
o 0.001*
0.16*
0.98*
0.88*
0.11*
0.97*
0.893
Data presented as %, unless otherwise specified.
CDR = Clinical Dementia Rating; D = Alzheimer’s disease; GDS = Geriatric Depression Scale; SD = standard deviation.
* w2 test.
Braz J Psychiatry. 2020;42(3)
290
NB Araujo et al.
Table 2 Measures based on ROC curve analysis in the total sample
AUC (95%CI)
Optimal
cutoff point
Sensitivity
(%)
Specificity
(%)
Correctly
classified (%)
LR+
LR-
General cognitive function
RUDAS (n=135)
0.87 (0.82-0.93)
p 23/30
81.54
76.06
78.68
3.41
0.24
Memory
RPT-immediate learning (n=135)
RPT-delayed recall (n=135)
RPT-recognition (n=135)
ECR (n=134)
0.93
0.93
0.79
0.93
(0.89-0.97)
(0.89-0.98)
(0.72-0.86)
(0.88-0.97)
p 18
p5
p 10
p 12
81.54
90.77
86.15
89.23
87.14
91.43
70.00
84.06
84.44
91.11
77.78
86.57
6.34
10.59
2.87
5.59
0.21
0.10
0.19
0.13
Language
Picture naming (n=135)
VF (n=135)
SF (n=135)
0.59 (0.53-0.66)
0.76 (0.68-0.84)
0.89 (0.85-0.94)
p 10
p 13
p 14
90.77
66.15
78.46
27.14
77.46
78.57
57.78
72.00
78.52
1.25
2.9
3.66
0.34
0.43
0.27
Executive functions
CTT 1 (n=120)
FDT 1 (n=121)
FDT 2 (n=119)
FDT 3 (n=120)
FDT 4 (n=116)
Serial threes (n=134)
0.74
0.66
0.61
0.63
0.63
0.61
(0.65-0.83)
(0.56-0.76)
(0.51-0.71)
(0.53-0.73)
(0.53-0.73)
(0.52-0.70)
p 99
p 36
p 38
p 59
p 82
p6
80.73
63.16
60.94
64.29
57.41
59.38
65.50
60.94
59.66
64.06
58.06
62.86
72.50
61.98
58.18
64.17
57.76
61.19
2.31
1.62
1.49
1.79
1.37
1.59
0.29
0.60
0.69
0.56
0.73
0.65
Visuospatial function
Copying of simple figures (n=134)
Semicomplex figure copy (n=98)
CDT (n=133)
0.72 (0.63- 0.80)
0.73 (0.63- 0.83)
0.82 (0.75-0.89)
p 05
p 20
p 04
60.94
69.57
71.88
73.61
73.08
86.96
67.65
71.43
79.70
2.30
2.58
5.5
0.53
0.42
0.32
Measure
95%CI = 95% confidence interval; AUC = area under the receiver operating characteristic (ROC) curve; CDT = Clock Drawing Test;
CRT = Clock Reading Test; CTT = Color Trails Test; ECR = Enhanced Cued Recall; FDT = Five Digit Test; LR- = negative likelihood ratio;
LR+ = positive likelihood ratio; n = sample; RPT = Recall of Pictures Test; RUDAS = Rowland Universal Dementia Assessment Scale;
SF = supermarket fluency; VF = verbal fluency (animal).
Table 3 Measures based on ROC curve analysis in low schooling participants
AUC (95%CI)
Optimal
cutoff point
Sensitivity
(%)
Specificity
(%)
Correctly
classified (%)
LR+
LR-
General cognitive function
RUDAS (n=69)
0.82 (0.72-0.91)
p 23
67.74
79.00
73.91
3.21
0.41
Memory
RPT-immediate learning (n=69)
RPT-delayed recall (n=69)
RPT-recognition (n=6)
ECR (n=6)
0.88
0.87
0.76
0.88
(0.81-0.96)
(0.78-0.96)
(0.64-0.87)
(0.79-0.96)
p 16
p4
p 10
p 12
80.65
87.10
77.42
80.65
78.95
84.21
73.68
83.78
79.71
85.51
75.36
82.35
3.83
5.51
2.94
4.97
0.25
0.15
0.31
0.23
Language
Picture naming (n=69)
VF (n=69)
SF (n=69)
0.58 (0.49-0.68)
0.67 (0.54-0.80)
0.83 (0.75-0.93)
N/S
p 12
p 14
54.84
74.19
73.68
78.95
65.22
76.81
2.08
3.52
0.61
0.33
Executive functions
CTT 1 (n=58)
FDT 1 (n=61)
FDT 2 (n=60)
FDT 3 (n=60)
FDT 4 (n=57)
Serial threes (n=68)
0.56
0.55
0.50
0.43
0.48
0.45
(0.40-0.71)
(0.40-0.69)
(0.35-0.65)
(0.29-0.58)
(0.32-0.63)
(0.32-0.59)
N/S
N/S
N/S
N/S
N/S
N/S
Visuospatial function
Simple copying test-cross (n=69)
Semicomplex figure copy (n=36)
CDT (n=67)
CRT (N=67)
0.64
0.48
0.75
0.61
(0.51-0.77)
(0.28-0.68)
(0.64-0.86)
(0.48-0.75)
p 04
N/S
p 03
p4
51.61
73.68
63.77
1.96
0.66
56.67
61.29
83.78
55.56
71.64
58.21
3.49
1.38
0.51
0.69
Measure
Data presented as %, unless otherwise specified.
95%CI = 95% confidence interval; AUC = area under the receiver operating characteristic (ROC) curve; CDT = Clock Drawing Test;
CRT = Clock Reading Test; CTT = Color Trails Test; ECR = Enhanced Cued Recall; FDT = Five Digit Test; LR- = negative likelihood ratio;
LR+ = positive likelihood ratio; n = sample; N/S = not significant; RPT = Recall of Pictures Test; RUDAS = Rowland Universal Dementia
Assessment Scale;
SF = supermarket fluency; VF = verbal fluency (animal).
Braz J Psychiatry. 2020;42(3)
Diagnostic accuracy of CNTB-BR
291
Table 4 Measures based on ROC curve analysis in high schooling participants
AUC (95%CI)
Optimal
cutoff point
Sensitivity
(%)
Specificity
(%)
Correctly
classified (%)
LR+
LR-
General cognitive function
RUDAS (n=67)
0.92 (0.86-0.99)
p 24
91.18
81.82
86.57
5.00
0.11
Memory
RPT-immediate learning (n=66)
RPT-delayed recall (n=66)
RPT-recognition (n=66)
ECR (n=66)
Semicomplex figure recall (n=62)
0.98
0.99
0.81
0.97
0.99
(0.94-1.00)
(0.99-1.00)
(0.72-0.90)
(0.95-1.00)
(0.97-1.00)
p 21
p5
p 10
p 12
p 12
91.18
100.00
94.12
97.06
92.86
100.00
93.75
65.63
84.38
93.33
95.45
96.97
80.30
90.91
93.10
29.18
16.00
2.74
6.21
13.93
0.08
0.00
0.08
0.03
0.08
Language
Picture naming (n=66)
VF (n=67)
SF (n=66)
0.59 (0.52-0.67)
0.82 (0.72-0.92)
0.95 (0.89-0.99)
p 10
p 14
p 15
97.06
82.35
82.35
21.88
72.73
81.25
60.61
77.61
81.82
1.24
3.02
4.39
0.13
0.24
0.22
Executive functions
CTT 1 (n=62)
CTT 2 (n=53)
FDT 1 (n=60)
FDT 2 (n=59)
FDT 3 (n=60)
FDT 4 (n=59)
Serial threes (n=66)
0.89
0.84
0.73
0.69
0.80
0.73
0.76
(0.81-0.98)
(0.71-0.96)
(0.59-0.87)
(0.54-0.84)
(0.69-0.91)
(0.59-0.87)
(0.66-0.87)
p 95
p 141
p 32
p 32
p 57
p 75
p6
78.57
80.00
65.38
72.00
61.54
64.00
85.29
88.24
78.79
79.41
61.76
85.29
64.71
62.50
83.87
79.25
73.33
66.10
75.00
64.41
74.24
6.68
3.77
3.18
1.88
4.18
1.81
2.27
0.24
0.25
0.44
0.45
0.45
0.56
0.24
Visuospatial function
Copying of simple figures (n=67)
Semicomplex figure copy (n=62)
CDT (n=66)
CRT (n=63)
0.79
0.86
0.89
0.89
(0.68-0.89)
(0.77-0.95)
(0.80-0.97)
(0.81-0.97)
p 06
p 21
p 04
p 9.5
63.64
86.67
94.12
79.41
82.35
71.88
78.13
79.31
73.13
79.03
86.36
79.37
3.61
3.08
4.30
3.84
0.44
0.19
0.08
0.26
Measure
Data presented as %, unless otherwise specified.
95%CI = 95% confidence interval; AUC = area under the receiver operating characteristic (ROC) curve; CDT = Clock Drawing Test;
CRT = Clock Reading Test; CTT = Color Trails Test; ECR = Enhanced Cued Recall; FDT = Five Digit Test; LR- = negative likelihood ratio;
LR+ = positive likelihood ratio; n = sample; RPT = Recall of Pictures Test; RUDAS = Rowland Universal Dementia Assessment Scale;
SF = supermarket fluency; VF = verbal fluency (animal).
to schooling level. Schooling influenced measures of
executive function and visuoconstruction ability.
SF scores o14 detected dementia with a sensitivity of
74.19%, a specificity of 78.95%, LR+ of 3.52 and LR- of
0.33 (Table 3, Figure 1) in the low education group. SF
scores o15 classified AD with a sensitivity of 82.35% and
a specificity of 81.25% in the high schooling group (Table 4,
Figure 1). RPT-named scores o10 detected dementia with
sensitivity of 83.87% and specificity of 31.58% in the low
schooling group (Table 3), and RPT-named scores o10
classified AD with a sensitivity of 97.06% and specificity
of 21.88% in the high schooling group (Table 4). RPTdelayed recall scores o4 detected dementia with a sensitivity of 87.10% and specificity of 84.21% in the low
schooling group (Table 3, Figure 2), and RPT-delayed
recall scores o5 classified AD with a sensitivity of 100%
and specificity of 93.75% in the high schooling group
(Table 4, Figure 2). RPT-recognition scores o10 detected
dementia with a sensitivity of 77.42% and specificity of
73.68% in the low schooling group (Table 3, Figure 3), and
RPT-recognition scores o10 classified AD with a sensitivity of 94.12% and specificity of 65.63% in the high
schooling group (Table 4, Figure 3). Finally, ECR scores
o12 detected dementia with a sensitivity of 80.65% and
specificity of 83.78% in the low schooling group (Table 3,
Figure 4), and ECR scores o12 classified AD with a
sensitivity of 97.06% and specificity of 84.38% in the high
schooling group (Table 4, Figure 4).
Discussion
This article addresses the translation, diagnostic accuracy, and standardized version of the CNTB for use in
Brazil, considering the educational level of a sample of
older adults with and without AD. To the best of our knowledge, this study is the first to use all subscale battery and
to consider the effect of schooling in a Brazilian Portuguese speaking sample with different levels of formal
education. The results indicate that the CNTB is useful for
speakers of Brazilian Portuguese with different cultural
characteristics, as has also been confirmed in a recent
study in Europe.12
The CNTB was developed to minimize the influence of
culture, language, and educational level.13 In this study,
the tests that were least impacted by schooling were
RUDAS, SF, RPT Picture naming, delayed recall and
recognition, and ECR. Like us, Nielsen et al.12 found that
the RPT and ECR were unaffected by schooling.
In SF, the optimal cutoff shows little variation between
the different schooling levels. Also, in line with our results,
other studies have found that the SF is less affected by
education, and that it is more ecologically relevant for
Braz J Psychiatry. 2020;42(3)
292
NB Araujo et al.
Figure 1 Receiver operating characteristic (ROC) curve for
the supermarket fluency (SF) test. A) ROC curve for SF in
subjects with low education (p 4 years of schooling). B)
ROC curve for SF in subjects with high education (X 8 years
of schooling).
illiterate individuals.32,33 Nielsen et al.23,24 have also
investigated the cross-cultural applicability of the RPT
in samples of Turkish immigrants and Danish elderly.
Despite being a short and simple test, the RPT is useful
for specific evaluation of memory, with low impact of
schooling. Nitrini et al.22 developed a similar test to the
BCSB; the performance of illiterate and literate participants did not differ in the BCSB memory test. The optimal
cutoff for diagnostic accuracy using the ECR does not
vary for the comparison between the total sample, low,
or high schooling. Another study34 evaluated the performance of a Turkish sample in ECR; in that study, again
schooling did not affect the ECR results.
The present study found significantly poorer performance of the low schooling group compared to the high
schooling group in executive function and visuoconstruction. Based on the present findings, the optimal cutoff for
diagnostic accuracy using the VF, CTT1, FDT, CDT,
Braz J Psychiatry. 2020;42(3)
Figure 2 Receiver operating characteristic (ROC) curve
for the Recall of Pictures Test (RPT)-delayed recall. A)
ROC curve for the RPT-delayed recall in subjects with
low education (p 4 years of schooling). B) ROC curve for
the RPT-delayed recall in subjects with high education
(X 8 years of schooling).
CRT, and copying of simple figures does substantially
vary with schooling. The high levels of schooling group
performed better than the low levels of schooling group.
Conversely, RUDAS, RPT, ECR, picture naming, and SF
performances were largely unaffected by education.
Similarly to the present study, a report by Nielsen
et al.35 investigated the performance of illiterate and
literate Turkish immigrants on the CNTB. The preliminary
findings suggest that illiteracy status affected measures of
mental processing speed, executive function, and visuoconstruction. In turn, memory measures relying on free
and cued recall, recognition of pictures, naming of colored
pictures, and SF were relatively unaffected by illiteracy.
This study has some limitations that should be acknowledged. The current sample included only participants at
Diagnostic accuracy of CNTB-BR
Figure 3 Receiver operating characteristic (ROC) curve for
the Recall of Pictures Test (RPT)-delayed recognition. A)
ROC curve for the RPT-delayed recognition for subjects with
low education (p 4 years of schooling). B) ROC curve for
the RPT-delayed recognition for subjects with high education
(X 8 years of schooling).
Figure 4 Receiver operating characteristic (ROC) curve for
the Enhanced Cued Recall (ECR). A) ROC curve for the
ECR in subjects with low education (p 4 years of schooling).
B) ROC curve for the ECR in subjects with high education
(X 8 years of schooling).
mild or moderate stages of dementia. Thus, the findings
do not apply for evaluation of persons with severe
dementia. In addition, the sample was selected from an
outpatient setting; and our pilot study only included four
participants. Another limitation is that we did not include
patients with mild cognitive impairment (MCI), even though
this a group will also come to clinics for assessment of
dementia. In addition, people with depression were
excluded – another limitation, given the high prevalence
of comorbidity with mild dementia. Finally, the GDS-15 was
only administered to assess depressive symptoms in the
AD group. Future research should consider depressive
symptoms in dementia reported by caregivers. Also, MCI
participants should be included in future studies. Therefore, replication of this study in a community-based sample
is important.
The CNTB has demonstrated feasibility for application
in Brazil, and appears to be appropriate for evaluating
different cognitive domains, including global cognitive
function, memory, executive functions, visuospatial functions, and language. The cognitive tests less affected by
schooling level were RUDAS, SF, RPT-naming, delayed
recall, recognition, and ECR. The cognitive tests that best
discriminated patients with AD from controls were RPTdelayed recall and ECR, both of which evaluate memory.
Based on these features, the use of the CNTB may
improve the cognitive assessment of AD and healthy
elderly; and CNTB may be useful to discriminate between
older adults with and without dementia, with high and low
schooling.
In Brazil, few validated instruments are available for
cognitive assessment of persons with low schooling.
293
Braz J Psychiatry. 2020;42(3)
294
NB Araujo et al.
There is a need for reliable methods to detect cognitive
deficits that can be used in these populations across cultural scenarios. Thus, the CNTB seems adequate for use in
a context with the rich cultural diversity found in Brazil.
Acknowledgements
Funding was provided by Fundac¸ão Carlos Chagas Filho
de Amparo à Pesquisa do Estado do Rio de Janeiro
(FAPERJ) (edital FAPERJ no. 06/2013, Programa PróIdoso – Apoio ao Estudo de Temas Relacionados à Saúde
e Cidadania de Pessoas Idosas – 2013, FAPERJ, E-26/
110.069/2013). JL is researcher 2 from Conselho Nacional
de Desenvolvimento Cientı́fico e Tecnológico (CNPq) and
Cientista do Nosso Estado from FAPERJ (2018-2020).
The authors thank neuropsychologists Marcos Avellar
and Michelle Scipião, psychiatrist Annibal Truzzi, and
students Matheus Jardim, Thaı́s Campinho, Renata Naylor,
Bruna Alves, and Marcelo Ferreira for the support with data
collection.
Disclosure
The authors report no conflicts of interest.
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