cognition - neuropsychological tests - dementia - long term memory - episodic memory
- mild cognitive impairment
cognição - teste neuropsicológico - demencia - memoria de longo prazo - memoria episódica
- comprometimento cognitivo leve
One of the most frequent and substantial complaints regarding cognition in the older
population is related to changes in memory. Deficits in memory tests, especially in
episodic long-term memory, have the highest sensibility for the neuropsychological
diagnosis of dementia[1] and amnestic mild cognitive impairment (MCI).
The greatest difficulties in assessing the memory of older subjects regarding the
clinical diagnosis of dementia or MCI occur when the subjects evaluated are illiterate,
have minimal formal education, or already have significant memory deficits. A flexible
and beneficial instrument to assess memory would provide a better ability to aid in
the early diagnosis of dementia, especially if the instrument is not very long or
difficult and has instructions that are easy to understand.
The Fuld Object Memory Evaluation (FOME)[2],[3] is an instrument that assesses learning and memory and incorporates selective-reminding
procedures. It has been incorporated in dementia research in different countries in
populations with different durations of formal education as a measure of overall recall
because it has simple instructions and seems easier to the patients because they touch
and see the objects that must be memorised, and the objects are very simple and well
known[4],[5],[6],[7],[8].
In an interesting study, FOME was one of the 4 instruments used in a combination of
cognitive tests and informant reports of dementia screening in low educated older
people. The combination of these 4 instruments, FOME, Mini-Mental State Examination
(MMSE), Informant Questionnaire of Cognitive Decline (IQCODE) and Bayer-Activities
of Daily Living Scale (B-ADL); with the mixed rule correctly classified 100% and the
logistic regression classified 95.7% of a Brazilian sample subjects. This combination
proved useful to improve the screening of mild to moderate dementia in low educated
older people[9].
The objective of the present study was to provide normative data on the FOME test
for the Brazilian elderly population and to investigate the influence of education,
age and sex on episodic memory performance. Our hypothesis was that subjects who had
less education would perform worse than those who had more years of education, younger
subjects would perform better than older subjects, and sex would have no effect on
performance.
METHOD
The normative sample consisted of 2,132 older subjects with normal cognitive performance
selected as part of a two-phase epidemiological study to investigate the prevalence
of dementia in a community-based sample in Sao Paulo and Ribeirao Preto, Brazil. Data
for this study were select between 2002 and 2003[10].
Sample selection
According to the Brazilian Institute of Geography and Statistics (IBGE) in 2000, São
Paulo is the largest city in Brazil, and the city’s population is 10,426,384, of whom
9.3% are 60 years old or older. Ribeirao Preto is a city in southeastern Brazil with
a population of approximately 500,000, and 10.1% of the population is aged sixty years
and older.
A clustered random sampling of a population of individuals aged 60 years old and older
from three different socioeconomic classes (upper, middle and low) was used, following
official census data[11],[12]. This strategy aimed to evaluate a sample containing city districts that represent
the area universe context of elderly individuals living in Sao Paulo and Ribeirao
Preto. Initially, the 96 city districts were ranked from the wealthiest to the poorest
according to data from the 2000 Census, provided by IBGE. The following parameters
were applied: income, education, proportion of elderly living in each district and
sanitation. Subsequently, the districts were divided into three groups, and a district
that was representative of each socioeconomic stratum was chosen to represent the
upper, middle and lower group.
In Sao Paulo, those three selected districts (upper, middle and lower class) had 17,186;
17,738 and 14,443 elderly individuals, respectively. Then, blocks of 10 homes were
randomly chosen in each of the 90 selected census sectors. Following local media (newspaper,
radio, television) and mail advertisement, a trained team started a systematic door-knocking
survey, visiting 8,042 homes to find elderly subjects. After the identification of
elderly subjects, a sample of 2,233 subjects older than 60 years of age was approached
in the community, and a total of 1,563 subjects who agreed to be visited by a trained
interviewer (response rate = 70%) were assessed. The interviewers tried at least three
times to evaluate the elderly subjects at home before they were considered to have
refused. The socio-demographic characteristics of the sample assessed at home have
been presented in greater detail recently[13], but the mean age was 71.4 years (60 to 102; SD = 8.03), 68.7% were female, 16.6%
were illiterate, and 71.0% had up to 8 years of education.
In Ribeirao Preto, a sample of 1,828 subjects were approached, of whom 1,145 agreed
to participate (683 subjects refused to participate; rate of attrition: 37.3%). The
sample came from three socio-economic levels in the following fashion: upper class:
369 subjects (32.2% of the total sample); middle class: 439 subjects (38.3%); lower
class: 332 subjects (29%); data were missing for five subjects.
The sample had a mean age of 70.9 years (60 to 100; SD = 7.7), 63.4% were female,
10.1% were illiterate, and 62.2% had up to 8 years of education[14].
In the first phase of this study, subjects were screened for dementia with a combination
of cognitive tests and functional scales: the MMSE[15], the Brazilian version of the FOME and a semantic verbal fluency examination were
administered to the patients. The IQCODE[16]and the B-ADL[17] were also administered to the informants. Depressive symptoms were evaluated with
a 10-item instrument, the D-10 (scores from 0 to 10), which contains questions related
to the presence of depressive symptoms most of the time during the past 2 weeks[18].
The following instruments were also used: socio-demographic questionnaire and socioeconomic
classification scale (allowing five levels of classification). Data were obtained
directly from the cognitively intact elderly subjects and/or from an informant, who
was usually a close relative, when the subject was cognitively impaired. Data were
collected at the participants’ homes between July, 2002 and August, 2003.
All individuals with positive screenings for dementia and depression and a random
sample of negative screenings were invited for the second phase, where clinical evaluation
and diagnosis were achieved by the consensus of at least two physicians and consistency
with the DSM-IV (American Psychiatric Association, 1994)[19] criteria for psychiatric diagnosis.
All subjects considered negative after screenings in the community phase and all subjects
evaluated in the second phase who were considered free of psychiatric diagnoses were
considered for the present investigation. Moreover, to guarantee the inclusion of
normal cognitive subjects, we excluded subjects with a MMSE ≤ 18[20],[21] and IQCODE ≤ 3.37[22], resulting in a sample of 2,132 elderly subjects. This sample was then stratified
for education, age and sex. Education was categorized into four groups: no formal
education, 1 to 4 years of formal education, 5 to 8 years, and 9 and above years of
formal education. Age was divided into three groups: 60 to 69, 70 to 79, and above
80 years of age.
The investigation was approved by the local ethics committee, and all of the subjects
agreed to participate in the study by signing the informed consent.
Fuld Object Memory Evaluation
The FOME is an instrument used to evaluate several components of learning and memory
in elderly people, and it also provides information about tactile recognition, right-left
discrimination, and verbal fluency. Ten common objects in a bag (ball, button, matchbox,
pacifiers, spoon, toothbrush, pencil, comb, catch, cup) are presented to the subjects
to determine whether he can identify objects by touch, alternating systematically
right and left hand. The patient name each object and then pulls it out of the bag
to see if he was right. After conducting a distracting task by asking the patient
to say words rapidly from a semantic category, “things that make people happy” (1
minute), the subject is asked to recall the items from the bag. After each recall,
he is slowly and clearly reminded verbally of each item omitted in that trial, for
a total of 5 trials. A 30-sec rapid semantic retrieval trail comes after each learning
trail as a distractor for the next recall trial. The categories for these distractor
trials are respectively, “animals”, “fruits”, “food”, “give name” (same sex as the
patient) and “things that make people sad”. After a 15 minutes interval filled by
other tests, an unexpected final recall is requested. Then, a multiple choice recognition
task is elicited only for those items not recalled.
The Brazilian version of the test uses all the same semantic categories of the original
version, with the exception of “vegetables “, which was changed to “fruits”. In the
original version the ten objects in the bag are; ball, bottle, button, card, cup,
key, matches, nail, ring, scissors, that were changed by the previously listed objects.
The data collected during the test are classified as follows: Immediate retrievalis determined by the total sum of items remembered in all trials; the storage efficiencyis determined by the number of different items recalled over the 5 trials and the
retrieval efficiency is determined by the total number of items recalled in successive trails without
any reminding. Delayed recall is the number of items remembered spontaneously after an interval.
Statistical analysis
The statistical analysis was based on the crude means and standard deviations (SD)
of the FOME scores and on the frequencies and percentages of socio-demographic variables.
The comparisons of FOME performance by sex was carried out by independent t-test and
the comparison by age and educational level were carried out by one-way Analysis of
Variance (ANOVA) followed by Tukey’s post-hoc tests. Normality of distribution was
verified using the Kolmogorov-Smirnov test.
The factors associated with memory score were analysed by multiple linear regression
models with FOME score as dependent variable and education, age and sex as independent
variables. The initial multivariate model included all variables and its interactions.
In the final model, only those variables/interactions that maintained an association
with FOME score at a level of 0.05 or less were retained. Same significance level
of a = 0.05 was used for all other comparisons, and the statistical analysis was performed
using the Statistical Package for Social Sciences (SPSS) for Windows, version 14.0.
RESULTS
For descriptive purposes, years of education were divided into four groups, and age
was divided into three age ranges.
[Table 1] shows the socio-demographic characteristics of the sample.
Table 1
Socio-demographic and clinical characteristics of the sample.
|
Frequency (%)
|
Mean (SD)
|
Range (min; max)
|
Education (years)
|
|
|
|
Illiteracy
|
213 (10.0)
|
|
|
1-4
|
880 (41.3)
|
|
|
5-8
|
260 (12.2)
|
|
|
≥ 9
|
779 (36.5)
|
|
|
Age (years)
|
|
|
|
60-69
|
1,069 (50.1)
|
|
|
70-79
|
797 (37.4)
|
|
|
≥ 80
|
257 (12.1)
|
|
|
Sex
|
|
|
|
Male
|
726 (34.1%)
|
|
|
Female
|
1,406 (65.9%)
|
|
|
MMSE
|
|
26.48 (3.26)
|
(18; 50)
|
IQCODE
|
|
3.03 (0.26)
|
(1; 3.37)
|
BADL
|
|
1.68 (1.22)
|
(0.92; 24)
|
|
Total
|
2,132
|
|
|
SD: Standard Deviation; MMSE: Mini-Mental State Examination; IQCODE: Informant Questionnaire
of Cognitive Decline and BADL: Bayer-Activities of Daily Living Scale.
[Table 2] shows the mean and standard deviation (SD) of the FOME scores, immediate total recall,
delayed recall, recognition and verbal fluency scores between sex. In general, females
presented higher scores (except in verbal fluency animal and sad, and recognition).
Table 2
Mean, standard deviation (SD) and p-values comparing FOME performance between sex.
|
Male Mean (SD)
|
Female Mean (SD)
|
Total Mean (SD)
|
p*
|
Immediate retrieval
|
37.43 (6.82)
|
39.40 (6.50)
|
38.73 (6.68)
|
< 0.001
|
Verbal fluency 1 – happy
|
4.26 (1.85)
|
4.53 (1.98)
|
4.45 (1.94)
|
0.002
|
Verbal fluency 2 – animal
|
11.30 (3.65)
|
11.09 (3.69)
|
11.16 (3.68)
|
0.199
|
Verbal fluency 3 – fruits
|
8.40 (1.89)
|
8.84 (2.00)
|
8.69 (1.97)
|
< 0.001
|
Verbal fluency 4 – names
|
8.50 (2.40)
|
8.82 (2.45)
|
8.70 (2.43)
|
0.005
|
Verbal Fluency 5 – sad
|
3.92 (1.76)
|
4.08 (1.88)
|
4.02 (1.84)
|
0.059
|
Delayed recall
|
8.06 (1.66)
|
8.55 (1.60)
|
8.38 (1.64)
|
< 0.001
|
Recognition
|
9.86 (0.82)
|
9.94 (0.41)
|
9.92 (0.54)
|
0.013
|
* independent t-test. FOME: Fuld Object Memory Evaluation.
[Table 3] shows the mean and SD of the FOME scores, immediate total recall, delayed recall,
recognition and verbal fluency scores in the three different age groups. The FOME
score decreased with advancing age with statistical significance (except in recognition).
Table 3
Mean, standard deviation (SD) and p-values comparing FOME performance between age
categories.
|
60-69 Mean (SD)
|
70-79 Mean (SD)
|
≥ 80 Mean (SD)
|
Total Mean (SD)
|
p*
|
Immediate retrieval
|
40.10a(5.99)
|
38.13b (6.61)
|
34.84c(7.79)
|
38.73(6.68)
|
< 0.001
|
Verbal fluency 1 – happy
|
4.55a(1.99)
|
4.39ab(1.91)
|
4.20b(1.82)
|
4.45 (1.94)
|
0.017
|
Verbal fluency 2 – animal
|
11.55a(3.94)
|
10.87b(3.35)
|
10.44b(3.28)
|
11.16 (3.68)
|
< 0.001
|
Verbal fluency 3 – fruits
|
8.84a(1.91)
|
8.63a(1.93)
|
8.26b(2.24)
|
8.69 (1.97)
|
< 0.001
|
Verbal fluency 4 – names
|
8.96a(2.42)
|
8.59b(2.40)
|
8.00c(2.43)
|
8.70 (2.43)
|
< 0.001
|
Verbal Fluency 5 – sad
|
4.08a(1.80)
|
3.95a(1.92)
|
4.00a(1.73)
|
4.02 (1.84)
|
0.294
|
Delayed recall
|
8.66a(1.45)
|
8.24b(1.68)
|
7.70c(1.96)
|
8.38 (1.64)
|
< 0.001
|
Recognition
|
9.93a(0.53)
|
9.91a(0.63)
|
9.85a(0.63)
|
9.92 (0.54)
|
0.114
|
* One-way Analysis of Variance with Tukey post-hoc. Groups with same superscript letter
are not significantly different (p > 0.05). FOME: Fuld Object Memory Evaluation.
[Table 4] shows mean and SD for the FOME scores, immediate total recall, delayed recall, recognition
and verbal fluency scores in the three different education levels. Data show that
FOME scores increased with increasing years of education with statistical significance.
Table 4
Mean, standard deviation (SD) and p-values comparing FOME performance between education
categories.
|
0 Mean (SD)
|
1-4 Mean (SD)
|
5-8 Mean (SD)
|
≥ 9 Mean (SD)
|
Total Mean (SD)
|
p*
|
Immediate retrieval
|
36.67a(6.80)
|
37.83a(6.37)
|
39.22b(6.84)
|
40.14a(6.61)
|
38.73 (6.67)
|
< 0.001
|
Verbal fluency 1 – happy
|
3.59a(1.45)
|
3.94a(1.63)
|
4.65b(1.93)
|
5.17c(2.12)
|
4.45 (1.94)
|
< 0.001
|
Verbal fluency 2 – animal
|
9.47a(2.82)
|
9.91a(3.01)
|
11.73b(3.50)
|
12.84c(3.88)
|
11.16 (3.68)
|
< 0.001
|
Verbal fluency 3 – fruits
|
7.56a(1.73)
|
8.19b(1.78)
|
9.21c(2.15)
|
9.39c(1.87)
|
8.69 (1.97)
|
< 0.001
|
Verbal fluency 4 – names
|
7.50a(2.14)
|
8.09b(2.21)
|
9.15c(2.56)
|
9.58c(2.37)
|
8.70 (2.43)
|
< 0.001
|
Verbal Fluency 5 – sad
|
3.09a(1.34)
|
3.51b(1.63)
|
4.26c(1.67)
|
4.76d(1.94)
|
4.02 (1.84)
|
< 0.001
|
Delayed recall
|
7.98a(1.77)
|
8.18a(1.56)
|
8.50b(1.66)
|
8.69b(1.63)
|
8.38 (1.64)
|
< 0.001
|
Recognition
|
9.91a(0.47)
|
9.93a(0.51)
|
9.95a(0.37)
|
9.89a(0.73)
|
9.92 (0.54)
|
0.470
|
* One-way Analysis of Variance with Tukey post-hoc. Groups with same superscript letter
are not significantly different (p > 0.05). FOME: Fuld Object Memory Evaluation.
[Table 5] shows the percentiles of the FOMES’s immediate and delayed recall performance by
age and by education level.
Table 5
Derived scores for each normative group on the FOME immediate retrieval and delayed
retrieval.
Immediate retrieval
|
|
Percentile Scores
|
Age 60-69
|
Age 70-79
|
Age ≥ 80
|
|
Education (years)
|
Education (years)
|
Education (years)
|
|
illiteracy
|
1-4
|
5-8
|
≥ 9
|
illiteracy
|
1-4
|
5-8
|
≥ 9
|
illiteracy
|
1-4
|
5-8
|
≥ 9
|
n = 89
|
n = 445
|
n = 127
|
n = 165
|
n = 96
|
n = 331
|
n = 98
|
n = 118
|
n = 26
|
n = 97
|
n = 34
|
n = 36
|
90
|
45.00
|
46.00
|
47.00
|
47.00
|
44.00
|
45.00
|
46.00
|
47.00
|
43.00
|
43.20
|
43.00
|
46.60
|
75
|
44.00
|
43.00
|
45.00
|
45.00
|
41.00
|
42.00
|
44.00
|
44.00
|
39.25
|
40.50
|
40.25
|
43.75
|
50
|
39.00
|
40.00
|
42.00
|
42.00
|
36.00
|
38.00
|
40.50
|
40.00
|
35.50
|
36.00
|
36.00
|
41.00
|
25
|
35.00
|
35.00
|
38.00
|
38.50
|
32.00
|
33.00
|
36.00
|
35.00
|
29.50
|
29.50
|
27.75
|
35.50
|
10
|
29.00
|
31.00
|
31.80
|
34.60
|
27.00
|
29.00
|
31.00
|
29.00
|
25.40
|
23.80
|
22.00
|
25.70
|
|
Delayed retrieval recall
|
|
Percentile Scores
|
Age 60-69
|
Age 70-79
|
Age ≥ 80
|
|
Education (years)
|
Education (years)
|
Education (years)
|
|
illiteracy
|
1-4
|
5-8
|
≥ 9
|
illiteracy
|
1-4
|
5-8
|
≥ 9
|
illiteracy
|
1-4
|
5-8
|
≥ 9
|
|
n = 87
|
n = 439
|
n = 123
|
n = 163
|
n = 95
|
n = 333
|
n = 97
|
n = 117
|
n = 24
|
n = 96
|
n = 34
|
n = 36
|
|
90
|
10.00
|
10.00
|
10.00
|
10.00
|
10.00
|
10.00
|
10.00
|
10.00
|
10.00
|
10.00
|
10.00
|
10.00
|
75
|
10.00
|
10.00
|
10.00
|
10.00
|
9.00
|
9.00
|
10.00
|
10.00
|
10.00
|
9.00
|
9.00
|
9.75
|
50
|
9.00
|
9.00
|
9.00
|
9.00
|
8.00
|
8.00
|
9.00
|
9.00
|
8.00
|
8.00
|
8.00
|
8.50
|
25
|
7.00
|
8.00
|
8.00
|
8.00
|
7.00
|
7.00
|
7.00
|
8.00
|
7.00
|
7.00
|
6.00
|
7.00
|
10
|
6.00
|
6.00
|
7.00
|
7.00
|
5.60
|
6.00
|
7.00
|
6.00
|
5.50
|
5.00
|
4.5.
|
4.70
|
FOME: Fuld Object Memory Evaluation.
To identify the simultaneous effect of education, age and sex on the FOME scores,
a multiple linear regression analysis was performed and is displayed in [Table 6].
Table 6
Final results of the multiple linear regression of socio-demographic variables associated
to FOME score.
Socio-demographic variables
|
Beta value
|
Std. Error
|
95%CI
|
p-value
|
Intercept
|
9.261
|
0.101
|
(9.064; 9.458)
|
< 0.001
|
Education (years)
|
|
|
|
<0.001
|
No formal education
|
- 0.753
|
0.225
|
(-1.195; -0.311)
|
0.001
|
1-4
|
- 0.625
|
0.135
|
(- 0.891; -0.360)
|
< 0.001
|
5-8
|
- 0.485
|
0.198
|
(-0.873; -0.096)
|
0.014
|
≥ 9
|
0
|
|
|
|
Age (years)
|
|
|
|
< 0.001
|
60-69
|
0
|
|
|
|
70-79
|
- 0.478
|
0.161
|
(-0.783; -0.162)
|
0.003
|
≥ 80
|
- 1.473
|
0.218
|
(-1.901; -1.045)
|
< 0.001
|
Sex
|
|
|
|
< 0.001
|
Male
|
-0.655
|
0.162
|
(-0.971; -0.338)
|
< 0.001
|
Female
|
0
|
|
|
|
Age * Education
|
|
|
|
0.030
|
Age ≥ 80 * education 0
|
0.840
|
0.493
|
(-0.127; 1.807)
|
0.088
|
Age ≥ 80 * education 1-4
|
0.780
|
0.303
|
(0.186; 1.374)
|
0.010
|
Age ≥ 80 * education 5-8
|
0.549
|
0.410
|
(-0.256; 1.354)
|
0.181
|
Age ≥ 80 * education ≥ 9
|
0
|
|
|
|
Age 70-79 * education 0
|
-0.273
|
0.319
|
(-0.899; 0.353)
|
0.392
|
Age 70-79 * education 1-4
|
0.055
|
0.213
|
(-0.363; 0.472)
|
0.797
|
Age 70-79 * education 5-8
|
0.378
|
0.302
|
(0.215; 0.971)
|
0.212
|
Age 70-79 * education ≥ 9
|
0
|
|
|
|
Age 60-69 * education 0
|
0
|
|
|
|
Age 60-69 * education 1-4
|
0
|
|
|
|
Age 60-69 * education 5-8
|
0
|
|
|
|
Age 60-69 * education ≥ 9
|
0
|
|
|
|
In each variable, the category with Beta = 0 indicates the reference category.
Sex did not present significant interactions with sex and education. FOME: Fuld Object
Memory Evaluation.
The reference groups of women (sex), younger individuals (age) and participants with
higher education levels (education) were considered to provide better clinical interpretation
and all these three variables presented significant influence on the FOME score.
It was observed that the variables age and education presented significant interaction
(p = 0.03). However, there were no significant interactions of these variables with
sex (p > 0.05).
DISCUSSION
We analysed the performance of a Brazilian community-based sample of older subjects
drawn from two Brazilian cities on the FOME test. The main finding of the present
study is that the FOME test is influenced by education, age and sex.
Age and education are variables known to affect cognitive performance, so the influence
of these two variables on the FOME score is not surprising. Generally, aging affects
fluid intelligence, including episodic memory[23], and the influence of education on cognition is already well documented in the literature[24].
Our results regarding memory are in accordance with previous findings from Brazilian
studies, which also showed the influence of education and age on episodic memory tests.
One study that assessed verbal episodic memory in a sample of older adults documented
significant differences between literate and illiterate subjects[25]. Another study that assessed verbal and visual episodic memory in a sample of the
Brazilian population found that age and years of education had a significant influence
on the tests results. However, no significant influence of sex was observed[26]. The same influence was documented in the normative data of the word list test with
a health elderly sample, but again, no influence of sex was reported[27].
Brazilian data indicate that education has no influence on the FOME exit score, and
these data might be explained by sample characteristics, such as smaller sizes and
less heterogeneity regarding education attainment compared to the present community-based
sample[28],[29]. Regarding the influence of sex on the episode memory test, this result was not
expected based on results reported in the literature[26],[29].
Therefore, although the statistical analysis indicated that education influenced FOME
scores, the FOME remains suitable for use in older people with lower levels of education.
Another reason supporting its use is that it is a memory test during which even very
elderly patients with significant memory problems and individuals with very low formal
education typically do not complain or show anxiety. On the contrary, they enjoy the
test. A different reaction is frequently observed for word list tests, in that patients
sometimes refuse to perform them.
Our results corroborate a previous study, which showed that the FOME was a good test
for assessing older people with few years of schooling[30]. Another study in China found influences of age and education on the FOME performance
but less influence of sex in the older population[31].
The normative data are relevant due to the limited availability of memory tests standardised
for the Brazilian population; moreover, the data presented can help clinicians to
better interpret immediate and delayed scores on episodic memory tests in older Brazilians
with varying degrees of education from community-based or primary care samples. Our
results also support the notion that clinicians should carefully analyse the memory
test performance in low-education elderly populations with memory complaints.
In conclusion, data presented here can help clinicians to better diagnosis Brazilian
elderly with memory problems.
There is a limitation of this study, some classifications that the FOME test can provide,
storage and retrieval efficiency, could not be analysed in these study because on
the time of the data collect, these classifications were not tabulated.